Protein disulfide isomerase plasma levels in healthy humans reveal proteomic signatures involved in contrasting endothelial phenotypes

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Citações na Scopus
21
Tipo de produção
article
Data de publicação
2019
Editora
ELSEVIER SCIENCE BV
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ISSN da Revista
Título do Volume
Autores
GARCIA-ROSA, Sheila
SACHETTO, Ana Teresa Azevedo
MORETTI, Ana Iochabel Soares
SILVA, Nathalia Tenguan
MARTINS-DE-SOUZA, Daniel
SANTORO, Marcelo Larami
Autor de Grupo de pesquisa
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Citação
REDOX BIOLOGY, v.22, article ID UNSP 101142, 14p, 2019
Projetos de Pesquisa
Unidades Organizacionais
Fascículo
Resumo
Redox-related plasma proteins are candidate reporters of protein signatures associated with endothelial structure/function. Thiol-proteins from protein disulfide isomerase (PDI) family are unexplored in this context. Here, we investigate the occurrence and physiological significance of a circulating pool of PDI in healthy humans. We validated an assay for detecting PDI in plasma of healthy individuals. Our results indicate high inter-individual (median = 330 pg/mL) but low intra-individual variability over time and repeated measurements. Remarkably, plasma PDI levels could discriminate between distinct plasma proteome signatures, with PDI-rich ( > median) plasma differentially expressing proteins related to cell differentiation, protein processing, housekeeping functions and others, while PDI-poor plasma differentially displayed proteins associated with coagulation, inflammatory responses and immunoactivation. Platelet function was similar among individuals with PDI-rich vs. PDI-poor plasma. Remarkably, such protein signatures closely correlated with endothelial function and phenotype, since cultured endothelial cells incubated with PDI-poor or PDI-rich plasma recapitulated gene expression and secretome patterns in line with their corresponding plasma signatures. Furthermore, such signatures translated into functional responses, with PDI-poor plasma promoting impairment of endothelial adhesion to fibronectin and a disturbed pattern of wound-associated migration and recovery area. Patients with cardiovascular events had lower PDI levels vs. healthy individuals. This is the first study describing PDI levels as reporters of specific plasma proteome signatures directly promoting contrasting endothelial phenotypes and functional responses.
Palavras-chave
Protein disulfide isomerase, Plasma proteome, Endothelial cells, Plasma protein signatures, Thiol proteins
Referências
  1. Apperizeller-Herzog C, 2008, BBA-MOL CELL RES, V1783, P535, DOI 10.1016/j.bbamcr.2007.11.010
  2. Araujo TLS, 2017, REDOX BIOL, V12, P1004, DOI 10.1016/j.redox.2017.04.034
  3. Araujo TLS, 2017, FREE RADICAL BIO MED, V103, P199, DOI 10.1016/j.freeradbiomed.2016.12.021
  4. Badrichani AZ, 1999, J CLIN INVEST, V103, P543, DOI 10.1172/JCI2517
  5. Banfi C, 2005, PROTEOMICS, V5, P4443, DOI 10.1002/pmic.200402017
  6. Bekendam RH, 2016, NAT COMMUN, V7, DOI 10.1038/ncomms12579
  7. Bekendam RH, 2016, BASIC CLIN PHARMACOL, V119, P42, DOI 10.1111/bcpt.12573
  8. Bowley SR, 2017, NAT COMMUN, V8, DOI 10.1038/ncomms14151
  9. Cassoli JS, 2017, PROTEOMICS, V17, DOI 10.1002/pmic.201700209
  10. CHEN K, 1995, BRIT J HAEMATOL, V90, P425, DOI 10.1111/j.1365-2141.1995.tb05169.x
  11. CHEN K, 1992, BLOOD, V79, P2226
  12. Cho J, 2012, BLOOD, V120, P647, DOI 10.1182/blood-2011-08-372532
  13. Crescente M, 2016, ARTERIOSCL THROM VAS, V36, P1164, DOI 10.1161/ATVBAHA.116.307461
  14. Damgaard RB, 2011, DISCOV MED, V11, P221
  15. Druhan LJ, 2017, PLOS ONE, V12, DOI 10.1371/journal.pone.0170261
  16. Ellgaard L, 2005, EMBO REP, V6, P28, DOI 10.1038/sj.embor.7400311
  17. Essex DW, 2018, CURR OPIN HEMATOL, V25, P395, DOI 10.1097/MOH.0000000000000449
  18. Essex DW, 2009, ANTIOXID REDOX SIGN, V11, P1191, DOI [10.1089/ars.2008.2322, 10.1089/ARS.2008.2322]
  19. Essex DW, 1999, BIOCHEMISTRY-US, V38, P10398, DOI 10.1021/bi990694s
  20. Fan GQ, 2016, ONCOTARGET, V7, P83231, DOI 10.18632/oncotarget.13081
  21. Fernandes DC, 2009, ARCH BIOCHEM BIOPHYS, V484, P197, DOI 10.1016/j.abb.2009.01.022
  22. Flaumenhaft R, 2017, CURR OPIN HEMATOL, V24, P439, DOI 10.1097/MOH.0000000000000362
  23. Flaumenhaft R, 2016, BLOOD, V128, P893, DOI 10.1182/blood-2016-04-636456
  24. FREY EA, 1992, J EXP MED, V176, P1665, DOI 10.1084/jem.176.6.1665
  25. Ganz P, 2016, JAMA-J AM MED ASSOC, V315, P2532, DOI 10.1001/jama.2016.5951
  26. Garcia S, 2017, ADV EXP MED BIOL, V974, P193, DOI 10.1007/978-3-319-52479-5_15
  27. Giannakopoulos B, 2012, J AUTOIMMUN, V39, P121, DOI 10.1016/j.jaut.2012.05.005
  28. Han JY, 2016, REDOX BIOL, V9, P306, DOI 10.1016/j.redox.2016.09.003
  29. Hayashida K., 2018, CIRCULATION, V139
  30. Hudson DA, 2015, FREE RADICAL BIO MED, V80, P171, DOI 10.1016/j.freeradbiomed.2014.07.037
  31. Iqbal A, 2014, ARCH BIOCHEM BIOPHYS, V557, P72, DOI 10.1016/j.abb.2014.06.013
  32. Jannes CE, 2015, ATHEROSCLEROSIS, V238, P101, DOI 10.1016/j.atherosclerosis.2014.11.009
  33. Jasuja R, 2012, J CLIN INVEST, V122, P2104, DOI 10.1172/JCI61228
  34. Jasuja R, 2010, BLOOD, V116, P4665, DOI 10.1182/blood-2010-04-278184
  35. Jones AL, 2005, IMMUNOL CELL BIOL, V83, P106, DOI 10.1111/j.1440-1711.2005.01320.x
  36. Joshi A, 2018, CIRCULATION, V138, P2482, DOI 10.1161/CIRCULATIONAHA.118.036823
  37. Kim JM, 1997, SCIENCE, V278, P1954, DOI 10.1126/science.278.5345.1954
  38. Laurindo FRM, 2012, FREE RADICAL BIO MED, V52, P1954, DOI 10.1016/j.freeradbiomed.2012.02.037
  39. Lin L, 2015, J BIOL CHEM, V290, P23543, DOI 10.1074/jbc.M115.666180
  40. Montano SJ, 2014, ANAL BIOCHEM, V449, P139, DOI 10.1016/j.ab.2013.12.025
  41. Mor-Cohen R, 2016, ANTIOXID REDOX SIGN, V24, P16, DOI 10.1089/ars.2014.6149
  42. Moraes MS, 2014, ARCH BIOCHEM BIOPHYS, V558, P14, DOI 10.1016/j.abb.2014.06.011
  43. Moretti AIS, 2017, SCI REP-UK, V7, DOI 10.1038/s41598-017-16947-5
  44. Oliveira PVS, 2018, CLIN SCI, V132, P1257, DOI 10.1042/CS20180157
  45. Peixoto AS, 2018, J BIOL CHEM, V293, P1450, DOI 10.1074/jbc.M117.807016
  46. Pober JS, 2007, NAT REV IMMUNOL, V7, P803, DOI 10.1038/nri2171
  47. Prado GN, 2013, FASEB J, V27, P4619, DOI 10.1096/fj.13-228577
  48. Raturi A, 2007, FREE RADICAL BIO MED, V43, P62, DOI 10.1016/j.freeradbiomed.2007.03.025
  49. Raturi A, 2008, BBA-BIOMEMBRANES, V1778, P2790, DOI 10.1016/j.bbamem.2008.07.003
  50. Sharda A, 2018, EXPERT REV HEMATOL, V11, P437, DOI 10.1080/17474086.2018.1452612
  51. Sharda A, 2015, BLOOD, V125, P1633, DOI 10.1182/blood-2014-08-597419
  52. Moretti AIS, 2017, ARCH BIOCHEM BIOPHYS, V617, P106, DOI 10.1016/j.abb.2016.11.007
  53. Stopa JD, 2018, THROMB RES, V164, pS130, DOI 10.1016/j.thromres.2018.01.005
  54. Stopa JD, 2017, J BIOL CHEM, V292, P9063, DOI 10.1074/jbc.M116.771832
  55. Stopa JD, 2017, JCI INSIGHT, V2, DOI 10.1172/jci.insight.89373
  56. Sumpio BE, 2002, INT J BIOCHEM CELL B, V34, P1508, DOI 10.1016/S1357-2725(02)00075-4
  57. Tanaka LY, 2016, HYPERTENSION, V67, P613, DOI 10.1161/HYPERTENSIONAHA.115.06177
  58. Tang SQ, 1997, J BIOL CHEM, V272, P28704, DOI 10.1074/jbc.272.45.28704
  59. Thery Clotilde, 2006, Curr Protoc Cell Biol, VChapter 3, DOI 10.1002/0471143030.cb0322s30
  60. Tsuchida-Straeten N, 2005, J THROMB HAEMOST, V3, P865, DOI 10.1111/j.1538-7836.2005.01238.x
  61. Vegvari Akos, 2011, J Clin Bioinforma, V1, P24, DOI 10.1186/2043-9113-1-24
  62. Voigtlaender M, 2016, HAEMOPHILIA, V22, pE537, DOI 10.1111/hae.13074
  63. Wang L, 2015, FREE RADICAL BIO MED, V83, P305, DOI 10.1016/j.freeradbiomed.2015.02.007
  64. Xu SL, 2014, DRUG DISCOV TODAY, V19, P222, DOI 10.1016/j.drudis.2013.10.017
  65. Xu SL, 2012, P NATL ACAD SCI USA, V109, P16348, DOI 10.1073/pnas.1205226109
  66. Zhou JS, 2015, J CLIN INVEST, V125, P4391, DOI 10.1172/JCI80319