Effects of thrombospondin-4 on pro-inflammatory phenotype differentiation and apoptosis in macrophages.
Animals
Apoptosis
/ drug effects
Biomarkers
/ metabolism
Cell Survival
/ drug effects
Cytokines
/ metabolism
Inflammation
/ pathology
Inflammation Mediators
/ metabolism
Lipopolysaccharides
/ pharmacology
Macrophages, Peritoneal
/ drug effects
Mice
Mice, Inbred C57BL
Monocytes
/ drug effects
Peritonitis
/ pathology
Phenotype
Phosphorylation
/ drug effects
RAW 264.7 Cells
Recombinant Proteins
/ pharmacology
Thrombospondins
/ metabolism
Journal
Cell death & disease
ISSN: 2041-4889
Titre abrégé: Cell Death Dis
Pays: England
ID NLM: 101524092
Informations de publication
Date de publication:
23 01 2020
23 01 2020
Historique:
received:
28
05
2019
accepted:
07
10
2019
revised:
25
09
2019
entrez:
25
1
2020
pubmed:
25
1
2020
medline:
15
1
2021
Statut:
epublish
Résumé
Thrombospondin-4 (TSP-4) attracted renewed attention recently as a result of assignment of new functions to this matricellular protein in cardiovascular, muscular, and nervous systems. We have previously reported that TSP-4 promotes local vascular inflammation in a mouse atherosclerosis model. A common variant of TSP-4, P387-TSP-4, was associated with increased cardiovascular disease risk in human population studies. In a mouse atherosclerosis model, TSP-4 had profound effect on accumulation of macrophages in lesions, which prompted us to examine its effects on macrophages in more detail. We examined the effects of A387-TSP-4 and P387-TSP-4 on mouse macrophages in cell culture and in vivo in the model of LPS-induced peritonitis. In tissues and in cell culture, TSP-4 expression was associated with inflammation: TSP-4 expression was upregulated in peritoneal tissues in LPS-induced peritonitis, and pro-inflammatory signals, INFγ, GM-CSF, and LPS, induced TSP-4 expression in macrophages in vivo and in cell culture. Deficiency in TSP-4 in macrophages from Thbs4
Identifiants
pubmed: 31974349
doi: 10.1038/s41419-020-2237-2
pii: 10.1038/s41419-020-2237-2
pmc: PMC6978349
doi:
Substances chimiques
Biomarkers
0
Cytokines
0
Inflammation Mediators
0
Lipopolysaccharides
0
Recombinant Proteins
0
Thrombospondins
0
thrombospondin 4
0
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Langues
eng
Sous-ensembles de citation
IM
Pagination
53Subventions
Organisme : NCI NIH HHS
ID : R01 CA177771
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL117216
Pays : United States
Références
Adams, J. C. & Lawler, J. The thrombospondins. Int J. Biochem. Cell Biol. 36, 961 (2004).
pubmed: 15094109
pmcid: 2885884
doi: 10.1016/j.biocel.2004.01.004
Adams, J. C. & Lawler, J. The thrombospondins. Cold Spring Harb. Perspect. Biol. 3, a009712 (2011).
pubmed: 21875984
pmcid: 3179333
doi: 10.1101/cshperspect.a009712
Tan, F. L. et al. The gene expression fingerprint of human heart failure. Proc. Natl Acad. Sci. USA 99, 11387 (2002).
pubmed: 12177426
doi: 10.1073/pnas.162370099
pmcid: 12177426
Mustonen, E. et al. Thrombospondin-4 expression is rapidly upregulated by cardiac overload. Biochem. Biophys. Res. Commun. 373, 186 (2008).
pubmed: 18541142
doi: 10.1016/j.bbrc.2008.05.164
pmcid: 18541142
Frolova, E. G. et al. Thrombospondin-4 regulates fibrosis and remodeling of the myocardium in response to pressure overload. FASEB J. 26, 2363 (2012).
pubmed: 22362893
pmcid: 3360147
doi: 10.1096/fj.11-190728
Cingolani, O. H. et al. Thrombospondin-4 is required for stretch-mediated contractility augmentation in cardiac muscle. Circ. Res. 109, 1410 (2011).
pubmed: 22034490
pmcid: 3324097
doi: 10.1161/CIRCRESAHA.111.256743
Lynch, J. M. et al. A thrombospondin-dependent pathway for a protective ER stress response. Cell 149, 1257 (2012).
pubmed: 22682248
pmcid: 3372931
doi: 10.1016/j.cell.2012.03.050
Cho, J. Y. et al. Gene expression signature-based prognostic risk score in gastric cancer. Clin. Cancer Res. 17, 1850 (2011).
pubmed: 21447720
pmcid: 3078023
doi: 10.1158/1078-0432.CCR-10-2180
D’Errico, M. et al. Genome-wide expression profile of sporadic gastric cancers with microsatellite instability. Eur. J. Cancer 45, 461 (2009).
pubmed: 19081245
doi: 10.1016/j.ejca.2008.10.032
pmcid: 19081245
Singh, D. et al. Gene expression correlates of clinical prostate cancer behavior. Cancer Cell 1, 203 (2002).
pubmed: 12086878
doi: 10.1016/S1535-6108(02)00030-2
Ma, X. J. et al. A two-gene expression ratio predicts clinical outcome in breast cancer patients treated with tamoxifen. Cancer Cell 5, 607 (2004).
pubmed: 15193263
doi: 10.1016/j.ccr.2004.05.015
Curtis, C. et al. The genomic and transcriptomic architecture of 2,000 breast tumours reveals novel subgroups. Nature 486, 346 (2012).
pubmed: 22522925
pmcid: 3440846
doi: 10.1038/nature10983
Lu, X., Wang, Z. C., Iglehart, J. D., Zhang, X. & Richardson, A. L. Predicting features of breast cancer with gene expression patterns. Breast Cancer Res. Treat. 108, 191 (2008).
pubmed: 18297396
doi: 10.1007/s10549-007-9596-6
Frolova, E. G. et al. Thrombospondin-4 regulates vascular inflammation and atherogenesis. Circ. Res. 107, 1313 (2010).
pubmed: 20884877
pmcid: 2993182
doi: 10.1161/CIRCRESAHA.110.232371
Wessel, J., Topol, E. J., Ji, M., Meyer, J. & McCarthy, J. J. Replication of the association between the thrombospondin-4 A387P polymorphism and myocardial infarction. Am. Heart J. 147, 905 (2004).
pubmed: 15131549
doi: 10.1016/j.ahj.2003.12.013
McCarthy, J. J. et al. Large scale association analysis for identification of genes underlying premature coronary heart disease: cumulative perspective from analysis of 111 candidate genes. J. Med. Genet. 41, 334 (2004).
pubmed: 15121769
pmcid: 1579684
doi: 10.1136/jmg.2003.016584
Wilsgaard, T. et al. Clinically significant novel biomarkers for prediction of first ever myocardial infarction: the Tromso Study. Circ. Cardiovasc. Genet. 8, 363 (2015).
pubmed: 25613532
doi: 10.1161/CIRCGENETICS.113.000630
Topol, E. J. et al. Single nucleotide polymorphisms in multiple novel thrombospondin genes may be associated with familial premature myocardial infarction. Circulation 104, 2641 (2001).
pubmed: 11723011
doi: 10.1161/hc4701.100910
Yamada, Y. et al. Prediction of the risk of myocardial infarction from polymorphisms in candidate genes. N. Engl. J. Med. 347, 1916 (2002).
pubmed: 12477941
doi: 10.1056/NEJMoa021445
Kato, T. Y. A., Murase, Y., Hirashiki, A., Noda, A. & Yamada, Y. Specific gene polymorphisms could be risk factors for coronary artery disease in individuals with or without hypertention. Circulation (Suppl.) 108, IV–712 (2003).
Cui, J. et al. Gender dependent association of thrombospondin-4 A387P polymorphism with myocardial infarction. Arterioscler. Thromb. Vasc. Biol. 24, e183 (2004).
pubmed: 15528485
doi: 10.1161/01.ATV.0000147304.67100.ee
pmcid: 15528485
Cui, J. et al. Thrombospondin-4 1186G>C (A387P) is a sex-dependent risk factor for myocardial infarction: a large replication study with increased sample size from the same population. Am. Heart J. 152, 543 e541 (2006).
doi: 10.1016/j.ahj.2006.06.002
Kirk, J. A. & Cingolani, O. H. Thrombospondins in the transition from myocardial infarction to heart failure. J. Mol. Cell Cardiol. 90, 102 (2016).
pubmed: 26686988
doi: 10.1016/j.yjmcc.2015.12.009
pmcid: 26686988
Muppala, S. et al. Proangiogenic properties of thrombospondin-4. Arterioscler. Thromb. Vasc. Biol. 35, 1975 (2015).
pubmed: 26139464
pmcid: 4629500
doi: 10.1161/ATVBAHA.115.305912
Muppala, S. et al. Thrombospondin-4 mediates TGF-beta-induced angiogenesis. Oncogene 36, 5189 (2017).
pubmed: 28481870
pmcid: 5589494
doi: 10.1038/onc.2017.140
Turashvili, G. et al. Novel markers for differentiation of lobular and ductal invasive breast carcinomas by laser microdissection and microarray analysis. BMC Cancer 7, 55 (2007).
pubmed: 17389037
pmcid: 1852112
doi: 10.1186/1471-2407-7-55
McCart Reed, A. E. et al. Thrombospondin-4 expression is activated during the stromal response to invasive breast cancer. Virchows Arch. 463, 535 (2013).
pubmed: 23942617
doi: 10.1007/s00428-013-1468-3
pmcid: 23942617
Forster, S., Gretschel, S., Jons, T., Yashiro, M. & Kemmner, W. THBS4, a novel stromal molecule of diffuse-type gastric adenocarcinomas, identified by transcriptome-wide expression profiling. Mod. Pathol. 24, 1390 (2011).
pubmed: 21701537
doi: 10.1038/modpathol.2011.99
pmcid: 21701537
Su, F. et al. Over-expression of thrombospondin 4 correlates with loss of miR-142 and contributes to migration and vascular invasion of advanced hepatocellular carcinoma. Oncotarget 8, 23277 (2017).
pubmed: 28177895
pmcid: 5410303
Frolova, E. G. et al. Control of organization and function of muscle and tendon by thrombospondin-4. Matrix Biol. 37, 35 (2014).
pubmed: 24589453
pmcid: 4150858
doi: 10.1016/j.matbio.2014.02.003
Vanhoutte, D. et al. Thrombospondin expression in myofibers stabilizes muscle membranes. eLife 5, 17589 (2016).
doi: 10.7554/eLife.17589
Eroglu, C. et al. Gabapentin receptor alpha2delta-1 is a neuronal thrombospondin receptor responsible for excitatory CNS synaptogenesis. Cell 139, 380 (2009).
pubmed: 19818485
pmcid: 2791798
doi: 10.1016/j.cell.2009.09.025
Yang, H. J. et al. Thrombospondin-4 promotes neuronal differentiation of NG2 cells via the ERK/MAPK pathway. J. Mol. Neurosci. 60, 517 (2016).
pubmed: 27647309
doi: 10.1007/s12031-016-0845-1
pmcid: 27647309
Benner, E. J. et al. Protective astrogenesis from the SVZ niche after injury is controlled by Notch modulator Thbs4. Nature 497, 369 (2013).
pubmed: 23615612
pmcid: 3667629
doi: 10.1038/nature12069
Andersson, D. et al. Plasticity response in the contralesional hemisphere after subtle neurotrauma: gene expression profiling after partial deafferentation of the hippocampus. PLoS ONE 8, e70699 (2013).
pubmed: 23936241
pmcid: 3723880
doi: 10.1371/journal.pone.0070699
Girard, F., Eichenberger, S. & Celio, M. R. Thrombospondin 4 deficiency in mouse impairs neuronal migration in the early postnatal and adult brain. Mol. Cell Neurosci. 61, 176 (2014).
pubmed: 24983516
doi: 10.1016/j.mcn.2014.06.010
pmcid: 24983516
Pluskota, E. et al. Mechanism and effect of thrombospondin-4 polymorphisms on neutrophil function. Blood 106, 3970 (2005).
pubmed: 16099885
pmcid: 1895095
doi: 10.1182/blood-2005-03-1292
Brody, M. J. et al. Defective flux of thrombospondin-4 through the secretory pathway impairs cardiomyocyte membrane stability and causes cardiomyopathy. Mol. Cell Biol. 38, e00114 (2018).
pubmed: 29712757
pmcid: 6024163
doi: 10.1128/MCB.00114-18
Congote, L. F., Difalco, M. R. & Gibbs, B. F. The C-terminal peptide of thrombospondin-4 stimulates erythroid cell proliferation. Biochem. Biophys. Res. Commun. 324, 673 (2004).
pubmed: 15474480
doi: 10.1016/j.bbrc.2004.09.107
pmcid: 15474480
Park, J. et al. Central mechanisms mediating thrombospondin-4-induced pain states. J. Biol. Chem. 291, 13335 (2016).
pubmed: 27129212
pmcid: 4933243
doi: 10.1074/jbc.M116.723478
Crosby, N. D. et al. Thrombospondin-4 and excitatory synaptogenesis promote spinal sensitization after painful mechanical joint injury. Exp. Neurol. 264, 111 (2015).
pubmed: 25483397
doi: 10.1016/j.expneurol.2014.11.015
Stenina, O. I. et al. Thrombospondin-4 and its variants: expression and differential effects on endothelial cells. Circulation 108, 1514 (2003).
pubmed: 12952849
doi: 10.1161/01.CIR.0000089085.76320.4E
Dunkle, E. T., Zaucke, F. & Clegg, D. O. Thrombospondin-4 and matrix three-dimensionality in axon outgrowth and adhesion in the developing retina. Exp. Eye Res. 84, 707 (2007).
pubmed: 17320079
doi: 10.1016/j.exer.2006.12.014
Narouz-Ott, L., Maurer, P., Nitsche, D. P., Smyth, N. & Paulsson, M. Thrombospondin-4 binds specifically to both collagenous and non-collagenous extracellular matrix proteins via its C-terminal domains. J. Biol. Chem. 275, 37110 (2000).
pubmed: 10956668
doi: 10.1074/jbc.M007223200
pmcid: 10956668
Kim, D. S. et al. Thrombospondin-4 contributes to spinal sensitization and neuropathic pain states. J. Neurosci. 32, 8977 (2012).
pubmed: 22745497
pmcid: 3408211
doi: 10.1523/JNEUROSCI.6494-11.2012
Subramanian, A. & Schilling, T. F. Thrombospondin-4 controls matrix assembly during development and repair of myotendinous junctions. eLife 3, e02372 (2014).
pmcid: 4096842
doi: 10.7554/eLife.02372
Pan, B. et al. Thrombospondin-4 divergently regulates voltage-gated Ca
pubmed: 27168360
pmcid: 4988923
doi: 10.1097/j.pain.0000000000000612
Arber, S. & Caroni, P. Thrombospondin-4, an extracellular matrix protein expressed in the developing and adult nervous system promotes neurite outgrowth. J. Cell Biol. 131, 1083 (1995).
pubmed: 7490284
doi: 10.1083/jcb.131.4.1083
Stenina, O. I. et al. Polymorphisms A387P in thrombospondin-4 and N700S in thrombospondin-1 perturb calcium binding sites. FASEB J. 19, 1893 (2005).
pubmed: 16148025
doi: 10.1096/fj.05-3712fje
Brody, M. J. et al. Dissection of thrombospondin-4 domains involved in intracellular adaptive endoplasmic reticulum stress-responsive signaling. Mol. Cell Biol. 36, 2 (2016).
pubmed: 26459760
Murray, P. J. & Wynn, T. A. Protective and pathogenic functions of macrophage subsets. Nat. Rev. Immunol. 11, 723 (2011).
pubmed: 21997792
pmcid: 3422549
doi: 10.1038/nri3073
Wynn, T. A., Chawla, A. & Pollard, J. W. Macrophage biology in development, homeostasis and disease. Nature 496, 445 (2013).
pubmed: 23619691
pmcid: 3725458
doi: 10.1038/nature12034
Colin, S., Chinetti-Gbaguidi, G. & Staels, B. Macrophage phenotypes in atherosclerosis. Immunol. Rev. 262, 153 (2014).
pubmed: 25319333
doi: 10.1111/imr.12218
Porta, C., Riboldi, E., Ippolito, A. & Sica, A. Molecular and epigenetic basis of macrophage polarized activation. Semin. Immunol. 27, 237 (2015).
pubmed: 26561250
doi: 10.1016/j.smim.2015.10.003
Ginhoux, F., Schultze, J. L., Murray, P. J., Ochando, J. & Biswas, S. K. New insights into the multidimensional concept of macrophage ontogeny, activation and function. Nat. Immunol. 17, 34 (2016).
pubmed: 26681460
doi: 10.1038/ni.3324
Murray, P. J. Macrophage polarization. Annu. Rev. Physiol. 79, 541 (2017).
pubmed: 27813830
doi: 10.1146/annurev-physiol-022516-034339
Benoit, M., Desnues, B. & Mege, J. L. Macrophage polarization in bacterial infections. J. Immunol. 181, 3733 (2008).
pubmed: 18768823
doi: 10.4049/jimmunol.181.6.3733
Kockx, M. M. Apoptosis in the atherosclerotic plaque: quantitative and qualitative aspects. Arterioscler. Thromb. Vasc. Biol. 18, 1519 (1998).
pubmed: 9763521
doi: 10.1161/01.ATV.18.10.1519
Kockx, M. M. et al. Cell composition, replication, and apoptosis in atherosclerotic plaques after 6 months of cholesterol withdrawal. Circ. Res. 83, 378 (1998).
pubmed: 9721694
doi: 10.1161/01.RES.83.4.378
Kockx, M. M. et al. Apoptosis and related proteins in different stages of human atherosclerotic plaques. Circulation 97, 2307 (1998).
pubmed: 9639374
doi: 10.1161/01.CIR.97.23.2307
pmcid: 9639374
Kockx, M. M. & Herman, A. G. Apoptosis in atherogenesis: implications for plaque destabilization. Eur. Heart J. 19(Suppl G), G23 (1998).
pubmed: 9717052
pmcid: 9717052
Kolodgie, F. D. et al. Localization of apoptotic macrophages at the site of plaque rupture in sudden coronary death. Am. J. Pathol. 157, 1259 (2000).
pubmed: 11021830
pmcid: 1850160
doi: 10.1016/S0002-9440(10)64641-X
Soler, C. et al. Lipopolysaccharide-induced apoptosis of macrophages determines the up-regulation of concentrative nucleoside transporters Cnt1 and Cnt2 through tumor necrosis factor-alpha-dependent and -independent mechanisms. J. Biol. Chem. 276, 30043 (2001).
pubmed: 11346649
doi: 10.1074/jbc.M101807200
pmcid: 11346649
Tabas, I. Macrophage death and defective inflammation resolution in atherosclerosis. Nat. Rev. Immunol. 10, 36 (2010).
pubmed: 19960040
doi: 10.1038/nri2675
pmcid: 19960040
Xaus, J. et al. LPS induces apoptosis in macrophages mostly through the autocrine production of TNF-alpha. Blood 95, 3823 (2000).
pubmed: 10845916
doi: 10.1182/blood.V95.12.3823.012k07_3823_3831
pmcid: 10845916
Lawler, P. R. & Lawler, J. Molecular basis for the regulation of angiogenesis by thrombospondin-1 and -2. Cold Spring Harb. Perspect. Med. 2, a006627 (2012).
pubmed: 22553494
pmcid: 3331684
doi: 10.1101/cshperspect.a006627
Lawler, J. Thrombospondin-1 as an endogenous inhibitor of angiogenesis and tumor growth. J. Cell Mol. Med. 6, 1 (2002).
pubmed: 12003665
pmcid: 6740251
doi: 10.1111/j.1582-4934.2002.tb00307.x
Shapouri-Moghaddam, A. et al. Macrophage plasticity, polarization, and function in health and disease. J. Cell Physiol. 233, 6425 (2018).
pubmed: 29319160
doi: 10.1002/jcp.26429
pmcid: 29319160
Hamilton, T. A., Zhao, C., Pavicic, P. G. Jr & Datta, S. Myeloid colony-stimulating factors as regulators of macrophage polarization. Front. Immunol. 5, 554 (2014).
pubmed: 25484881
pmcid: 4240161
doi: 10.3389/fimmu.2014.00554