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


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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.

About the authors

Xiaoxuan Zhang

Hebei Province Key Laboratory of Occupational Health and Safety for Coal Industry, School of Public Health, North China University of Science and Technology

Email: info@benthamscience.net

Ke Han

Hebei Province Key Laboratory of Occupational Health and Safety for Coal Industry, School of Public Health, North China University of Science and Technology

Email: info@benthamscience.net

Linhui Kan

Hebei Province Key Laboratory of Occupational Health and Safety for Coal Industry, School of Public Health, North China University of Science and Technology

Email: info@benthamscience.net

Zheng Zhang

Hebei Province Key Laboratory of Occupational Health and Safety for Coal Industry, School of Public Health, China University of Science and Technology

Email: info@benthamscience.net

Yihong Gong

Hebei Province Key Laboratory of Occupational Health and Safety for Coal Industry, School of Public Health, North China University of Science and Technology

Email: info@benthamscience.net

Shuyu Xiao

, Tangshan Center of Disease Control and Prevention

Email: info@benthamscience.net

Yuping Bai

Hebei Province Key Laboratory of Occupational Health and Safety for Coal Industry, School of Public Health, North China University of Science and Technology

Email: info@benthamscience.net

Nan Liu

Hebei Province Key Laboratory of Occupational Health and Safety for Coal Industry, School of Public Health, North China University of Science and Technology

Email: info@benthamscience.net

Chunyan Meng

Hebei Province Key Laboratory of Occupational Health and Safety for Coal Industry, School of Public Health, North China University of Science and Technology

Email: info@benthamscience.net

Huisheng Qi

, Tangshan City workers' Hospital

Author for correspondence.
Email: info@benthamscience.net

Fuhai Shen

Hebei Province Key Laboratory of Occupational Health and Safety for Coal Industry, School of Public Health, North China University of Science and Technology

Author for correspondence.
Email: info@benthamscience.net

References

  1. Leung, C.C.; Yu, I.T.S.; Chen, W. Silicosis. Lancet, 2012, 379(9830), 2008-2018. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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) doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 10.1111/jcmm.14083 PMID: 30843345

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