The Lipocalin2 Gene is Regulated in Mammary Epithelial Cells by NFκB and C/EBP In Response to Mycoplasma.
Animals
Binding Sites
CCAAT-Enhancer-Binding Proteins
/ metabolism
Epithelial Cells
/ metabolism
Gene Expression Regulation
Host-Pathogen Interactions
Humans
Lipocalin-2
/ genetics
Lipopeptides
/ metabolism
Mice
Mycoplasma
/ physiology
Mycoplasma Infections
/ genetics
NF-kappa B
/ metabolism
Protein Binding
Signal Transduction
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
06 05 2020
06 05 2020
Historique:
received:
27
08
2019
accepted:
25
03
2020
entrez:
8
5
2020
pubmed:
8
5
2020
medline:
1
12
2020
Statut:
epublish
Résumé
Lcn2 gene expression increases in response to cell stress signals, particularly in cells involved in the innate immune response. Human Lcn2 (NGAL) is increased in the blood and tissues in response to many stressors including microbial infection and in response to LPS in myeloid and epithelial cells. Here we extend the microbial activators of Lcn2 to mycoplasma and describe studies in which the mechanism of Lcn2 gene regulation by MALP-2 and mycoplasma infection was investigated in mouse mammary epithelial cells. As for the LPS response of myeloid cells, Lcn2 expression in epithelial cells is preceded by increased TNFα, IL-6 and IκBζ expression and selective reduction of IκBζ reduces Lcn2 promoter activity. Lcn2 promoter activation remains elevated well beyond the period of exposure to MALP-2 and is persistently elevated in mycoplasma infected cells. Activation of either the human or the mouse Lcn2 promoter requires both NFκB and C/EBP for activation. Thus, Lcn2 is strongly and enduringly activated by mycoplasma components that stimulate the innate immune response with the same basic regulatory mechanism for the human and mouse genes.
Identifiants
pubmed: 32376831
doi: 10.1038/s41598-020-63393-x
pii: 10.1038/s41598-020-63393-x
pmc: PMC7203223
doi:
Substances chimiques
CCAAT-Enhancer-Binding Proteins
0
Lipocalin-2
0
Lipopeptides
0
NF-kappa B
0
macrophage stimulatory lipopeptide 2
DZX5IUA94D
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
7641Subventions
Organisme : NIAID NIH HHS
ID : R21 AI114283
Pays : United States
Références
Yamazaki, S., Muta, T. & Takeshige, K. A novel IkappaB protein, IkappaB-zeta, induced by proinflammatory stimuli, negatively regulates nuclear factor-kappaB in the nuclei. J. Biol. Chem. 276, 27657–27662, https://doi.org/10.1074/jbc.M103426200 (2001).
doi: 10.1074/jbc.M103426200
pubmed: 11356851
Haruta, H., Kato, A. & Todokoro, K. Isolation of a novel interleukin-1-inducible nuclear protein bearing ankyrin-repeat motifs. J. Biol. Chem. 276, 12485–12488, https://doi.org/10.1074/jbc.C100075200 (2001).
doi: 10.1074/jbc.C100075200
pubmed: 11278262
Kitamura, H., Kanehira, K., Okita, K., Morimatsu, M. & Saito, M. MAIL, a novel nuclear I kappa B protein that potentiates LPS-induced IL-6 production. FEBS Lett. 485, 53–56, https://doi.org/10.1016/s0014-5793(00)02185-2 (2000).
doi: 10.1016/s0014-5793(00)02185-2
pubmed: 11086164
Playford, R. J. et al. Effects of Mouse and Human Lipocalin Homologues 24p3/lcn2 and Neutrophil Gelatinase-Associated Lipocalin on Gastrointestinal Mucosal Integrity and Repair. Gastroenterology 131, 809–817, https://doi.org/10.1053/j.gastro.2006.05.051 (2006).
doi: 10.1053/j.gastro.2006.05.051
pubmed: 16952550
Sola, A. et al. Sphingosine-1-phosphate signalling induces the production of Lcn-2 by macrophages to promote kidney regeneration. J. Pathol. 225, 597–608, https://doi.org/10.1002/path.2982 (2011).
doi: 10.1002/path.2982
pubmed: 22025214
Cai, L., Rubin, J., Han, W., Venge, P. & Xu, S. The Origin of Multiple Molecular Forms in Urine of HNL/NGAL. Clin. J. Am. Soc. Nephrology 5, 2229–2235, https://doi.org/10.2215/cjn.00980110 (2010).
doi: 10.2215/cjn.00980110
Liu, Q. & Nilsen-Hamilton, M. Identification of a new acute phase protein. J. Biol. Chem. 270, 22565–22570, https://doi.org/10.1074/jbc.270.38.22565 (1995).
doi: 10.1074/jbc.270.38.22565
pubmed: 7545679
Liu, Q., Ryon, J. & Nilsen-Hamilton, M. Uterocalin: A mouse acute phase protein expressed in the uterus around birth. Mol. Reprod. Dev. 46, 507–514, 10.1002/(SICI)1098-2795(199704)46:4<507::AID-MRD9>3.0.CO;2-S (1997).
Ryon, J., Bendickson, L. & Nilsen-Hamilton, M. High expression in involuting reproductive tissues of uterocalin/24p3, a lipocalin and acute phase protein. Biochemical J. 367, 271–277, https://doi.org/10.1042/BJ20020026 (2002).
doi: 10.1042/BJ20020026
Nilsen-Hamilton, M. et al. Tissue involution and the acute phase response. Ann. N. Y. Acad. Sci. 995, 94–108, https://doi.org/10.1111/j.1749-6632.2003.tb03213.x (2003).
doi: 10.1111/j.1749-6632.2003.tb03213.x
pubmed: 12814942
Sunil, V. R. et al. Acute endotoxemia is associated with upregulation of lipocalin 24p3/Lcn2 in lung and liver. Exp. Mol. Pathol. 83, 177–187, https://doi.org/10.1016/j.yexmp.2007.03.004 (2007).
doi: 10.1016/j.yexmp.2007.03.004
pubmed: 17490638
pmcid: 3954125
Hopfe, M., Deenen, R., Degrandi, D., Köhrer, K. & Henrich, B. Host cell responses to persistent mycoplasmas–different stages in infection of HeLa cells with Mycoplasma hominis. PLoS One 8, e54219, https://doi.org/10.1371/journal.pone.0054219 (2013).
doi: 10.1371/journal.pone.0054219
pubmed: 23326599
pmcid: 3543322
Waites, K. B., Xiao, L., Liu, Y., Balish, M. F. & Atkinson, T. P. Mycoplasma pneumoniae from the Respiratory Tract and Beyond. Clin. microbiology Rev. 30, 747–809, https://doi.org/10.1128/cmr.00114-16 (2017).
doi: 10.1128/cmr.00114-16
Bürki, S., Frey, J. & Pilo, P. Virulence, persistence and dissemination of Mycoplasma bovis. Veterinary Microbiology 179, 15–22, https://doi.org/10.1016/j.vetmic.2015.02.024 (2015).
doi: 10.1016/j.vetmic.2015.02.024
pubmed: 25824130
Rogers, M. B. Mycoplasma and cancer: in search of the link. Oncotarget 2, 271–273, https://doi.org/10.18632/oncotarget.264 (2011).
doi: 10.18632/oncotarget.264
pubmed: 21508438
pmcid: 3248167
Vande Voorde, J., Balzarini, J. & Liekens, S. Mycoplasmas and cancer: focus on nucleoside metabolism. EXCLI journal 13, 300-322, NA (2014).
Choi, H. S. et al. Detection of mycoplasma infection in circulating tumor cells in patients with hepatocellular carcinoma. Biochem. Biophys. Res. Commun. 446, 620–625, https://doi.org/10.1016/j.bbrc.2014.03.024 (2014).
doi: 10.1016/j.bbrc.2014.03.024
pubmed: 24637212
Duan, H. et al. Mycoplasma Hyorhinis Infection Promotes NF-B–Dependent Migration of Gastric Cancer Cells. Cancer Res. 74, 5782–5794, https://doi.org/10.1158/0008-5472.can-14-0650 (2014).
doi: 10.1158/0008-5472.can-14-0650
pubmed: 25136068
Duan, H., Qu, L. & Shou, C. Mycoplasma hyorhinis induces epithelial-mesenchymal transition in gastric cancer cell MGC803 via TLR4-NF-κB signaling. Cancer Lett. 354, 447–454, https://doi.org/10.1016/j.canlet.2014.08.018 (2014).
doi: 10.1016/j.canlet.2014.08.018
pubmed: 25149064
Patil, S., Rao, R. S. & Raj, A. T. Role of Mycoplasma in the Initiation and Progression of Oral Cancer. Journal of international oral health 7, i-ii, not assigned (2015).
Cao, S. et al. Potential malignant transformation in the gastric mucosa of immunodeficient mice with persistent Mycoplasma penetrans infection. PLoS One 12, e0180514, https://doi.org/10.1371/journal.pone.0180514 (2017).
doi: 10.1371/journal.pone.0180514
pubmed: 28692662
pmcid: 5503272
Ikehata, N. et al. Toll-like receptor 2 activation implicated in oral squamous cell carcinoma development. Biochem. Biophys. Res. Commun. 495, 2227–2234, https://doi.org/10.1016/j.bbrc.2017.12.098 (2018).
doi: 10.1016/j.bbrc.2017.12.098
pubmed: 29269299
Ye, H. et al. Association between genital mycoplasmas infection and human papillomavirus infection, abnormal cervical cytopathology, and cervical cancer: a systematic review and meta-analysis. Arch. Gynecol. Obstet. 297, 1377–1387, https://doi.org/10.1007/s00404-018-4733-5 (2018).
doi: 10.1007/s00404-018-4733-5
pubmed: 29520664
Zella, D. et al. Mycoplasma promotes malignant transformation in vivo, and its DnaK, a bacterial chaperone protein, has broad oncogenic properties. Proc. Natl Acad. Sci. USA 115, E12005–E12014, https://doi.org/10.1073/pnas.1815660115 (2018).
doi: 10.1073/pnas.1815660115
pubmed: 30509983
Zarei, O., Rezania, S. & Mousavi, A. Mycoplasma genitalium and cancer: a brief review. Asian Pac. J. Cancer Prev. 14, 3425–3428, https://doi.org/10.7314/apjcp.2013.14.6.3425 (2013).
doi: 10.7314/apjcp.2013.14.6.3425
pubmed: 23886122
Miyake, M. et al. Mycoplasma genitalium Infection and Chronic Inflammation in Human Prostate Cancer: Detection Using Prostatectomy and Needle Biopsy Specimens. Cells 8, 212, https://doi.org/10.3390/cells8030212 (2019).
doi: 10.3390/cells8030212
pmcid: 6468796
Barykova, Y. A. et al. Association of Mycoplasma hominis infection with prostate cancer. Oncotarget 2, 289–297, https://doi.org/10.18632/oncotarget.256 (2011).
doi: 10.18632/oncotarget.256
pubmed: 21471611
pmcid: 3248169
Mitin, V., Tumanova, L. & Botnariuc, N. Mycoplasma Faucium and Breast Cancer. bioRxiv, 089128, https://doi.org/10.1101/089128 (2016).
Razin, S., Yogev, D. & Naot, Y. Molecular biology and pathogenicity of mycoplasmas. Microbiology and molecular biology reviews 62, 1094–1156, not assigned (1998).
Galanos, C., Gumenscheimer, M., Muhlradt, P., Jirillo, E. & Freudenberg, M. MALP-2, a Mycoplasma lipopeptide with classical endotoxic properties: end of an era of LPS monopoly? J. Endotoxin Res. 6, 471–476 (2000).
doi: 10.1177/09680519000060061001
Knorr, C. et al. Macrophage-activating lipopeptide-2 (MALP-2) induces a localized inflammatory response in rats resulting in activation of brain sites implicated in fever. Brain Res. 1205, 36–46, https://doi.org/10.1016/j.brainres.2008.02.021 (2008).
doi: 10.1016/j.brainres.2008.02.021
pubmed: 18353287
Seya, T. & Matsumoto, M. A lipoprotein family from Mycoplasma fermentans confers host immune activation through Toll-like receptor 2. Int. J. Biochem. Cell Biol. 34, 901–906 (2002).
doi: 10.1016/S1357-2725(01)00164-9
Takeda, Y. et al. Type I Interferon-Independent Dendritic Cell Priming and Antitumor T Cell Activation Induced by a Mycoplasma fermentans Lipopeptide. Front. Immunol. 9, 496–496, https://doi.org/10.3389/fimmu.2018.00496 (2018).
doi: 10.3389/fimmu.2018.00496
pubmed: 29593736
pmcid: 5861346
Xu, Y. et al. Mycoplasma hyorhinis activates the NLRP3 inflammasome and promotes migration and invasion of gastric cancer cells. PLoS One 8, e77955, https://doi.org/10.1371/journal.pone.0077955 (2013).
doi: 10.1371/journal.pone.0077955
pubmed: 24223129
pmcid: 3819327
Deiters, U., Gumenscheimer, M., Galanos, C. & Muhlradt, P. F. Toll-like receptor 2- and 6-mediated stimulation by macrophage-activating lipopeptide 2 induces lipopolysaccharide (LPS) cross tolerance in mice, which results in protection from tumor necrosis factor alpha but in only partial protection from lethal LPS doses. Infect. Immun. 71, 4456–4462, https://doi.org/10.1128/iai.71.8.4456-4462.2003 (2003).
doi: 10.1128/iai.71.8.4456-4462.2003
pubmed: 12874325
pmcid: 166003
Luhrmann, A. et al. In vivo effects of a synthetic 2-kilodalton macrophage-activating lipopeptide of Mycoplasma fermentans after pulmonary application. Infect. Immun. 70, 3785–3792, https://doi.org/10.1128/iai.70.7.3785-3792.2002 (2002).
doi: 10.1128/iai.70.7.3785-3792.2002
pubmed: 12065522
pmcid: 128036
Omueti, K. O., Beyer, J. M., Johnson, C. M., Lyle, E. A. & Tapping, R. I. Domain exchange between human toll-like receptors 1 and 6 reveals a region required for lipopeptide discrimination. J. Biol. Chem. 280, 36616–36625, https://doi.org/10.1074/jbc.M504320200 (2005).
doi: 10.1074/jbc.M504320200
pubmed: 16129684
Rharbaoui, F. et al. The Mycoplasma-derived lipopeptide MALP-2 is a potent mucosal adjuvant. Eur J Immunol 32, 2857–2865, 10.1002/1521-4141(2002010)32:10<2857::AID-IMMU2857>3.0.CO;2-R (2002).
Borchsenius, S. N., Daks, A., Fedorova, O., Chernova, O. & Barlev, N. A. Effects of mycoplasma infection on the host organism response via p53/NF-κB signaling. J. Cell. Physiol. 234, 171–180, https://doi.org/10.1002/jcp.26781 (2019).
doi: 10.1002/jcp.26781
Gedye, C. et al. Mycoplasma Infection Alters Cancer Stem Cell Properties in Vitro. Stem Cell Rev. Rep. 12, 156–161, https://doi.org/10.1007/s12015-015-9630-8 (2016).
doi: 10.1007/s12015-015-9630-8
pubmed: 26514153
Zhang, H.-B., Fan, J.-M., Zhu, L.-L., Yuan, X.-H. & Shen, X.-W. Combination of NGAL and Cystatin C for Prediction of Preeclampsia at 10-14 Weeks of Gestation. Clin Lab 65, NA, https://doi.org/10.7754/Clin.Lab.2018.180831 (2019).
Tang, X.-Y. et al. Urine NGAL as an early biomarker for diabetic kidney disease: accumulated evidence from observational studies. Ren. Fail. 41, 446–454, https://doi.org/10.1080/0886022x.2019.1617736 (2019).
doi: 10.1080/0886022x.2019.1617736
pubmed: 31162999
pmcid: 6566833
Lu, J. et al. Serum NGAL Is Superior to Cystatin C in Predicting the Prognosis of Acute-on-Chronic Liver Failure. Ann. Hepatology 18, 155–164, https://doi.org/10.5604/01.3001.0012.7907 (2019).
doi: 10.5604/01.3001.0012.7907
Asimakopoulou, A., Borkham-Kamphorst, E., Tacke, F. & Weiskirchen, R. Lipocalin-2 (NGAL/LCN2), a “help-me” signal in organ inflammation. Hepatology 63, 669–671, https://doi.org/10.1002/hep.27930 (2016).
doi: 10.1002/hep.27930
pubmed: 26054053
Abella, V. et al. The potential of lipocalin-2/NGAL as biomarker for inflammatory and metabolic diseases. Biomarkers 20, 565–571, https://doi.org/10.3109/1354750x.2015.1123354 (2015).
doi: 10.3109/1354750x.2015.1123354
pubmed: 26671823
pmcid: 4819811
Hynes, N. E. et al. Epidermal growth factor receptor, but not c-erbB-2, activation prevents lactogenic hormone induction of the beta-casein gene in mouse mammary epithelial cells. Mol. Cell Biol. 10, 4027–4034, https://doi.org/10.1128/mcb.10.8.4027 (1990).
doi: 10.1128/mcb.10.8.4027
pubmed: 2196443
pmcid: 360913
Ball, R. K., Friis, R. R., Schoenenberger, C. A., Doppler, W. & Groner, B. Prolactin regulation of beta-casein gene expression and of a cytosolic 120-kd protein in a cloned mouse mammary epithelial cell line. EMBO J. 7, 2089–2095 (1988).
doi: 10.1002/j.1460-2075.1988.tb03048.x
Matsuo, S., Yamazaki, S., Takeshige, K. & Muta, T. Crucial roles of binding sites for NF-kappaB and C/EBPs in IkappaB-zeta-mediated transcriptional activation. Biochem. J. 405, 605–615, https://doi.org/10.1042/BJ20061797 (2007).
doi: 10.1042/BJ20061797
pubmed: 17447895
pmcid: 2267307
Cowland, J. B., Muta, T. & Borregaard, N. IL-1beta-specific up-regulation of neutrophil gelatinase-associated lipocalin is controlled by IkappaB-zeta. J. Immunol. 176, 5559–5566, https://doi.org/10.4049/jimmunol.176.9.5559 (2006).
doi: 10.4049/jimmunol.176.9.5559
pubmed: 16622025
Zahnow, C. A. CCAAT/enhancer binding proteins in normal mammary development and breast cancer. Breast Cancer Res. 4, 113–121, https://doi.org/10.1186/bcr428 (2002).
doi: 10.1186/bcr428
pubmed: 12052253
pmcid: 138725
Karlsen, J. R., Borregaard, N. & Cowland, J. B. Induction of Neutrophil Gelatinase-associated Lipocalin Expression by Co-stimulation with Interleukin-17 and Tumor Necrosis Factor-α Is Controlled by IκB-ζ but neither by C/EBP-β nor C/EBP-δ. J. Biol. Chem. 285, 14088–14100, https://doi.org/10.1074/jbc.M109.017129 (2010).
doi: 10.1074/jbc.M109.017129
pubmed: 20220144
pmcid: 2863242
Bolignano, D., Coppolino, G., Lacquaniti, A. & Buemi, M. From kidney to cardiovascular diseases: NGAL as a biomarker beyond the confines of nephrology. Eur. J. Clin. Invest. 40, 273–276, https://doi.org/10.1111/j.1365-2362.2010.02258.x (2010).
doi: 10.1111/j.1365-2362.2010.02258.x
pubmed: 20415702
Paragas, N. et al. The Ngal reporter mouse detects the response of the kidney to injury in real time. Nat. Med. 17, 216–222, https://doi.org/10.1038/nm.2290 (2011).
doi: 10.1038/nm.2290
pubmed: 21240264
pmcid: 3059503
Cernaro, V. et al. NGAL is a precocious marker of therapeutic response. Curr. Pharm. Des. 17, 844–849, https://doi.org/10.2174/138161211795428939 (2011).
doi: 10.2174/138161211795428939
pubmed: 21375495
McMahon, B. A. et al. Biomarker Predictors of Adverse Acute Kidney Injury Outcomes in Critically Ill Patients: The Dublin Acute Biomarker Group Evaluation Study. Am. J. Nephrology 50, 19–28, https://doi.org/10.1159/000500231 (2019).
doi: 10.1159/000500231
Park, H. S. et al. Urinary neutrophil gelatinase-associated lipocalin as a biomarker of acute kidney injury in sepsis patients in the emergency department. Clinica Chim. Acta 495, 552–555, https://doi.org/10.1016/j.cca.2019.06.005 (2019).
doi: 10.1016/j.cca.2019.06.005
Tidbury, N. et al. Neutrophil gelatinase-associated lipocalin as a marker of postoperative acute kidney injury following cardiac surgery in patients with pre-operative kidney impairment. Cardiovasc. Hematol. Disord. Drug. Targets 19, 1–10, https://doi.org/10.2174/1871529X19666190415115106 (2019).
doi: 10.2174/1871529X19666190415115106
Zhou, F., Luo, Q., Wang, L. & Han, L. Diagnostic value of neutrophil gelatinase-associated lipocalin for early diagnosis of cardiac surgery-associated acute kidney injury: a meta-analysis. Eur. J. Cardio-Thoracic Surg. 49, 746–755, https://doi.org/10.1093/ejcts/ezv199 (2016).
doi: 10.1093/ejcts/ezv199
Urbschat, A., Obermüller, N. & Haferkamp, A. Biomarkers of kidney injury. Biomarkers 16, S22–S30, https://doi.org/10.3109/1354750X.2011.587129 (2011).
doi: 10.3109/1354750X.2011.587129
pubmed: 21707441
Hamilton, R. T., Nilsen-Hamilton, M. & Adams, G. Superinduction by cycloheximide of mitogen-induced secreted proteins produced by Balb/c 3T3 cells. J. Cell Physiol. 123, 201–208, https://doi.org/10.1002/jcp.1041230208 (1985).
doi: 10.1002/jcp.1041230208
pubmed: 2579961
Nilsen-Hamilton, M., Hamilton, R. T. & Adams, G. A. Rapid selective stimulation by growth factors of the incorporation by BALB/C 3T3 cells of [35S]methionine into a glycoprotein and five superinducible proteins. Biochem. Biophys. Res. Commun. 108, 158–166, https://doi.org/10.1016/0006-291x(82)91845-9 (1982).
doi: 10.1016/0006-291x(82)91845-9
pubmed: 6216885
Cowland, J. B., Sorensen, O. E., Sehested, M. & Borregaard, N. Neutrophil gelatinase-associated lipocalin is up-regulated in human epithelial cells by IL-1 beta, but not by TNF-alpha. J. Immunol. 171, 6630–6639, https://doi.org/10.4049/jimmunol.171.12.6630 (2003).
doi: 10.4049/jimmunol.171.12.6630
pubmed: 14662866
Orabona, C., Dumoutier, L. & Renauld, J. C. Interleukin-9 induces 24P3 lipocalin gene expression in murine T cell lymphomas. Eur. Cytokine Netw. 12, 154–161 (2001).
pubmed: 11282560
Liu, Q. S., Nilsen-Hamilton, M. & Xiong, S. D. Synergistic regulation of the acute phase protein SIP24/24p3 by glucocorticoid and pro-inflammatory cytokines. Sheng Li Xue Bao 55, 525–529 (2003).
pubmed: 14566398
Zerega, B., Cermelli, S., Michelis, B., Cancedda, R. & Cancedda, F. D. Expression of NRL/NGAL (neu-related lipocalin/neutrophil gelatinase-associated lipocalin) during mammalian embryonic development and in inflammation. Eur J Cell Biol 79, 165–172, doi:not assigned (2000).
Vizzardelli, C. et al. Effects of dexamethazone on LPS-induced activation and migration of mouse dendritic cells revealed by a genome-wide transcriptional analysis. Eur. J. Immunol. 36, 1504–1515, https://doi.org/10.1002/eji.200535488 (2006).
doi: 10.1002/eji.200535488
pubmed: 16708398
Garay-Rojas, E., Harper, M., Hraba-Renevey, S. & Kress, M. An apparent autocrine mechanism amplifies the dexamethasone- and retinoic acid-induced expression of mouse lipocalin-encoding gene 24p3. Gene 170, 173–180, https://doi.org/10.1016/0378-1119(95)00896-9 (1996).
doi: 10.1016/0378-1119(95)00896-9
pubmed: 8666241
Du, X., Poltorak, A., Silva, M. & Beutler, B. Analysis of Tlr4-Mediated LPS Signal Transduction in Macrophages by Mutational Modification of the Receptor. Blood Cells, Molecules, Dis. 25, 328–338, https://doi.org/10.1006/bcmd.1999.0262 (1999).
doi: 10.1006/bcmd.1999.0262
Kitchens, R. L. & Munford, R. S. Enzymatically deacylated lipopolysaccharide (LPS) can antagonize LPS at multiple sites in the LPS recognition pathway. J. Biol. Chem. 270, 9904–9910, https://doi.org/10.1074/jbc.270.17.9904 (1995).
doi: 10.1074/jbc.270.17.9904
pubmed: 7537270
Huggins, T. et al. Quantitation of endotoxin and lipoteichoic acid virulence using toll receptor reporter gene. Am. J. Dent. 29, 321–327 (2016).
pubmed: 29178719
Muhlradt, P. F., Kiess, M., Meyer, H., Sussmuth, R. & Jung, G. Isolation, structure elucidation, and synthesis of a macrophage stimulatory lipopeptide from Mycoplasma fermentans acting at picomolar concentration. J. Exp. Med. 185, 1951–1958, https://doi.org/10.1084/jem.185.11.1951 (1997).
doi: 10.1084/jem.185.11.1951
pubmed: 9166424
pmcid: 2196331
Borregaard, N., Sehested, M., Nielsen, B. S., Sengelov, H. & Kjeldsen, L. Biosynthesis of granule proteins in normal human bone marrow cells. Gelatinase is. a marker terminal neutrophil differentiation. Blood 85, 812–817 (1995).
pubmed: 7833481
Flo, T. H. et al. Lipocalin 2 mediates an innate immune response to bacterial infection by sequestrating iron. Nature 432, 917–921, https://doi.org/10.1038/nature03104 (2004).
doi: 10.1038/nature03104
pubmed: 15531878
Srisawat, N., Murugan, R. & Kellum, J. A. Repair or progression after AKI: a role for biomarkers? Nephron Clin. Pract. 127, 185–189, https://doi.org/10.1159/000363254 (2014).
doi: 10.1159/000363254
pubmed: 25343847
Rebalka, I. A. et al. Loss of the adipokine lipocalin-2 impairs satellite cell activation and skeletal muscle regeneration. Am. J. Physiol. Cell Physiol 315, C714–C721, https://doi.org/10.1152/ajpcell.00195.2017 (2018).
doi: 10.1152/ajpcell.00195.2017
pubmed: 30257107
pmcid: 6293054
Thorsvik, S. et al. Ulcer-associated cell lineage expresses genes involved in regeneration and is hallmarked by high neutrophil gelatinase-associated lipocalin (NGAL) levels. J. Pathol. 248, 316–325, https://doi.org/10.1002/path.5258 (2019).
doi: 10.1002/path.5258
pubmed: 30746716
pmcid: 6618036
Jin, D., Zhang, Y. & Chen, X. Lipocalin 2 deficiency inhibits cell proliferation, autophagy, and mitochondrial biogenesis in mouse embryonic cells. Mol. Cell Biochem. 351, 165–172, https://doi.org/10.1007/s11010-011-0724-6 (2011).
doi: 10.1007/s11010-011-0724-6
pubmed: 21234651
Devireddy, L. R., Teodoro, J. G., Richard, F. A. & Green, M. R. Induction of apoptosis by a secreted lipocalin that is transcriptionally regulated by Il-3 deprivation. Science 293, 829–834, https://doi.org/10.1126/science.1061075 (2001).
doi: 10.1126/science.1061075
pubmed: 11486081
Liu, Z. et al. Multiple apoptotic defects in hematopoietic cells from mice lacking lipocalin 24p3. J. Biol. Chem. 286, 20606–20614, https://doi.org/10.1074/jbc.M110.216549 (2011).
doi: 10.1074/jbc.M110.216549
pubmed: 21507940
pmcid: 3121516
Wang, Y.-P. et al. Lipocalin-2 negatively modulates the epithelial-to-mesenchymal transition in hepatocellular carcinoma through the epidermal growth factor (TGF-beta1)/Lcn2/Twist1 pathway. Hepatology 58, 1349–1361, https://doi.org/10.1002/hep.26467 (2013).
doi: 10.1002/hep.26467
pubmed: 23696034
Liao, C.-J., Li, P.-T., Lee, Y.-C., Li, S.-H. & Chu, S. T. Lipocalin 2 induces the epithelial–mesenchymal transition in stressed endometrial epithelial cells: possible correlation with endometriosis development in a mouse model. Reproduction 147, 179–187, https://doi.org/10.1530/rep-13-0236 (2014).
doi: 10.1530/rep-13-0236
pubmed: 24194573
Lim, R. et al. Neutrophil gelatinase-associated lipocalin (NGAL) an early-screening biomarker for ovarian cancer: NGAL is associated with epidermal growth factor-induced epithelio-mesenchymal transition. Int. J. Cancer 120, 2426–2434, https://doi.org/10.1002/ijc.22352 (2007).
doi: 10.1002/ijc.22352
pubmed: 17294443
Nguyen, V. T. et al. Cutaneous wound healing in diabetic mice is improved by topical mineralocorticoid receptor blockade. Journal of Investigative Dermatology, https://doi.org/10.1016/j.jid.2019.04.030 (2019).
Peltier, M. R., Richey, L. J. & Brown, M. B. Placental lesions caused by experimental infection of Sprague-Dawley rats with Mycoplasma pulmonis. Am. J. Reprod. Immunol. 50, 254–262 (2003).
doi: 10.1034/j.1600-0897.2003.00075.x
Kennedy, S. & Ball, H. J. Pathology of experimental ureaplasma mastitis in ewes. Vet. Pathol. 24, 302–307, https://doi.org/10.1177/030098588702400403 (1987).
doi: 10.1177/030098588702400403
pubmed: 3617396
Rollins, S., Colby, T. & Clayton, F. Open lung biopsy in Mycoplasma pneumoniae pneumonia. Arch. Pathol. Lab. Med. 110, 34–41 (1986).
pubmed: 3753567
Lindsey, J. R. & Cassell, H. Experimental Mycoplasma pulmonis infection in pathogen-free mice. Models for studying mycoplasmosis of the respiratory tract. Am. J. Pathol. 72, 63–90 (1973).
pubmed: 4719529
pmcid: 1903941
Ibeagha-Awemu, E. M. et al. Bacterial lipopolysaccharide induces increased expression of toll-like receptor (TLR) 4 and downstream TLR signaling molecules in bovine mammary epithelial cells. Vet. Res. 39, 11, https://doi.org/10.1051/vetres:2007047 (2008).
doi: 10.1051/vetres:2007047
pubmed: 18096120
Pandey, S. & Agrawal, D. K. Immunobiology of Toll-like receptors: emerging trends. Immunol. Cell Biol. 84, 333–341, https://doi.org/10.1111/j.1440-1711.2006.01444.x (2006).
doi: 10.1111/j.1440-1711.2006.01444.x
pubmed: 16834572
Furrie, E., Macfarlane, S., Thomson, G. & Macfarlane, G. T. Toll-like receptors-2, −3 and −4 expression patterns on human colon and their regulation by mucosal-associated bacteria. Immunology 115, 565–574, https://doi.org/10.1111/j.1365-2567.2005.02200.x (2005).
doi: 10.1111/j.1365-2567.2005.02200.x
pubmed: 16011525
pmcid: 1782176
Muhlradt, P. F. & Frisch, M. Purification and partial biochemical characterization of a Mycoplasma fermentans-derived substance that activates macrophages to release nitric oxide, tumor necrosis factor, and interleukin-6. Infect. Immun. 62, 3801–3807 (1994).
doi: 10.1128/IAI.62.9.3801-3807.1994
Morr, M., Takeuchi, O., Akira, S., Simon, M. M. & Muhlradt, P. F. Differential recognition of structural details of bacterial lipopeptides by toll-like receptors. Eur J Immunol 32, 3337–3347, 10.1002/1521-4141(200212)32:12<3337::AID-IMMU3337>3.0.CO;2-# (2002).
Nathan, C. Points of control in inflammation. Nature 420, 846–852, https://doi.org/10.1038/nature01320 (2002).
doi: 10.1038/nature01320
pubmed: 12490957
Mellman, I. & Steinman, R. M. Dendritic cells: specialized and regulated antigen processing machines. Cell 106, 255–258, https://doi.org/10.1016/s0092-8674(01)00449-4 (2001).
doi: 10.1016/s0092-8674(01)00449-4
pubmed: 11509172
Barrenschee, M., Lex, D. & Uhlig, S. Effects of the TLR2 Agonists MALP-2 and Pam3Cys in Isolated Mouse Lungs. PLoS One 5, e13889, https://doi.org/10.1371/journal.pone.0013889 (2010).
doi: 10.1371/journal.pone.0013889
pubmed: 21124967
pmcid: 2987752
Kaufmann, A., Muhlradt, P. F., Gemsa, D. & Sprenger, H. Induction of cytokines and chemokines in human monocytes by Mycoplasma fermentans-derived lipoprotein MALP-2. Infect. Immun. 67, 6303–6308 (1999).
doi: 10.1128/IAI.67.12.6303-6308.1999
Osada, S., Yamamoto, H., Nishihara, T. & Imagawa, M. DNA Binding Specificity of the CCAAT/Enhancer-binding Protein Transcription Factor Family. J. Biol. Chem. 271, 3891–3896, https://doi.org/10.1074/jbc.271.7.3891 (1996).
doi: 10.1074/jbc.271.7.3891
pubmed: 8632009
Gombart, A. F. et al. Regulation of neutrophil and eosinophil secondary granule gene expression by transcription factors C/EBP epsilon and PU.1. Blood 101, 3265–3273, https://doi.org/10.1182/blood-2002-04-1039 (2003).
doi: 10.1182/blood-2002-04-1039
pubmed: 12515729
Du, Z.-P. et al. Neutrophil gelatinase-associated lipocalin in gastric carcinoma cells and its induction by TPA are controlled by C/EBPβ. Biochem. Cell Biol. 89, 314–324, https://doi.org/10.1139/o11-002 (2011).
doi: 10.1139/o11-002
pubmed: 21612443
Trapecar, M., Goropevsek, A., Gorenjak, M., Gradisnik, L. & Slak Rupnik, M. A co-culture model of the developing small intestine offers new insight in the early immunomodulation of enterocytes and macrophages by Lactobacillus spp. through STAT1 and NF-kB p65 translocation. PLoS One 9, e86297, https://doi.org/10.1371/journal.pone.0086297 (2014).
doi: 10.1371/journal.pone.0086297
pubmed: 24454965
pmcid: 3894201
Wright, F. L. et al. Hyperosmolarity invokes distinct anti-inflammatory mechanisms in pulmonary epithelial cells: evidence from signaling and transcription layers. PLoS One 9, e114129–e114129, https://doi.org/10.1371/journal.pone.0114129 (2014).
doi: 10.1371/journal.pone.0114129
pubmed: 25479425
pmcid: 4257597
Trask, O. J. Jr. Nuclear Factor Kappa B (NF-kappaB) Translocation Assay Development and Validation for High Content Screening. NBK100914 [bookaccession] (2004).
Kayama, H. et al. Class-specific regulation of pro-inflammatory genes by MyD88 pathways and IkappaBzeta. J. Biol. Chem. 283, 12468–12477, https://doi.org/10.1074/jbc.A115.709965 (2008).
doi: 10.1074/jbc.A115.709965
pubmed: 18319258
Kauf, A. C., Vinyard, B. T. & Bannerman, D. D. Effect of intramammary infusion of bacterial lipopolysaccharide on experimentally induced Staphylococcus aureus intramammary infection. Res. Vet. Sci. 82, 39–46, https://doi.org/10.1016/j.rvsc.2006.05.006 (2007).
doi: 10.1016/j.rvsc.2006.05.006
pubmed: 16887158
Hoff, F. W. et al. Mycoplasma contamination of leukemic cell lines alters protein expression determined by reverse phase protein arrays. Cytotechnology 70, 1529–1535, https://doi.org/10.1007/s10616-018-0244-2 (2018).
doi: 10.1007/s10616-018-0244-2
pubmed: 30191439
pmcid: 6269355
Yamamoto, M. et al. Regulation of Toll/IL-1-receptor-mediated gene expression by the inducible nuclear protein IkappaBzeta. Nature 430, 218–222, https://doi.org/10.1038/nature02738 (2004).
doi: 10.1038/nature02738
pubmed: 15241416
Danielson, K. G., Oborn, C. J., Durban, E. M., Butel, J. S. & Medina, D. Epithelial mouse mammary cell line exhibiting normal morphogenesis in vivo and functional differentiation in vitro. Proc. Natl Acad. Sci. USA 81, 3756–3760 (1984).
doi: 10.1073/pnas.81.12.3756
Bruchmuller, I. et al. Introduction of a validation concept for a PCR-based Mycoplasma detection assay. Cytotherapy 8, 62–69, https://doi.org/10.1080/14653240500518413 (2006).
doi: 10.1080/14653240500518413
pubmed: 16627346