Urine, peritoneal fluid and omental fat proteomes of reproductive age women: Endometriosis-related changes and associations with endocrine disrupting chemicals

Journal of Proteomics

Volumn 113, Issue , 2015, Pages 194-205

  Williams, Katherine E ^a,b   Miroshnychenko, Olga ^a   Johansen, Eric B ^a   Niles, Richard K ^a   Sundaram, Rajeshwari ^c   Kannan, Kurunthachalam ^d   Albertolle, Matthew ^a   Zhou, Yan ^a,b   Prasad, Namrata ^a,b   Drake, Penelope M ^a   Giudice, Linda C ^a,b   Hall, Steven C ^a,b   Witkowska, H Ewa ^a,b   Buck Louis, Germaine M ^c   Fisher, Susan J ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^d WADSWORTH CENTER   (United States)

Author keywords

Endometriosis; Environmental chemicals; Mass spectrometry; Omental fat; Peritoneal fluid; Urine

Indexed keywords

ENDOCRINE DISRUPTOR; FAT; GELATINASE B; LEUKOCYTE ELASTASE; PROTEIN FAM49B; PROTEOME; UNCLASSIFIED DRUG; MMP9 PROTEIN, HUMAN; ORAL CONTRACEPTIVE AGENT;

ARTICLE; ENDOMETRIOSIS; FEMALE; HUMAN; LIQUID CHROMATOGRAPHY; MAJOR CLINICAL STUDY; MASS SPECTROMETRY; NUCLEOTIDE SEQUENCE; OMENTUM; PERITONEAL FLUID; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN ANALYSIS; QUANTITATIVE ANALYSIS; URINE; ADIPOSE TISSUE; ADULT; ASCITES FLUID; CLINICAL TRIAL; METABOLISM; MULTICENTER STUDY; PATHOLOGY;

ADIPOSE TISSUE; ADULT; ASCITIC FLUID; CONTRACEPTIVES, ORAL, HORMONAL; ENDOMETRIOSIS; FEMALE; HUMANS; LEUKOCYTE ELASTASE; MATRIX METALLOPROTEINASE 9; OMENTUM; PROTEOME;

EID: 84908376996     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2014.09.015     Document Type: Article

References (61)

1. Albalat A., Mischak H., Mullen W. Urine proteomics in clinical applications: technologies, principal considerations and clinical implementation. Prilozi 2011, 32:13-44.
2. Prudent M., Tissot J.D., Lion N. Proteomics of blood and derived products: what's next?. Expert Rev Proteomics 2011, 8:717-737.
3. Vitorino R., Guedes S., Manadas B., Ferreira R., Amado F. Toward a standardized saliva proteome analysis methodology. J Proteomics 2012, 75:5140-5165.
4. May K.E., Conduit-Hulbert S.A., Villar J., Kirtley S., Kennedy S.H., Becker C.M. Peripheral biomarkers of endometriosis: a systematic review. Hum Reprod Update 2010, 16:651-674.
5. Rizner T.L. Noninvasive biomarkers of endometriosis: myth or reality?. Expert Rev Mol Diagn 2014, 14:365-385.
6. Fassbender A., Vodolazkaia A., Saunders P., Lebovic D., Waelkens E., De Moor B., et al. Biomarkers of endometriosis. Fertil Steril 2013, 99:1135-1145.
7. Cho S., Choi Y.S., Yim S.Y., Yang H.I., Jeon Y.E., Lee K.E., et al. Urinary vitamin D-binding protein is elevated in patients with endometriosis. Hum Reprod 2012, 27:515-522.
8. Yun B.H., Lee Y.S., Chon S.J., Jung Y.S., Yim S.Y., Kim H.Y., et al. Evaluation of elevated urinary enolase I levels in patients with endometriosis. Biomarkers 2014, 19:16-21.
9. Tokushige N., Markham R., Crossett B., Ahn S.B., Nelaturi V.L., Khan A., et al. Discovery of a novel biomarker in the urine in women with endometriosis. Fertil Steril 2011, 95:46-49.
10. Kuessel L., Jaeger-Lansky A., Pateisky P., Rossberg N., Schulz A., Schmitz A.A., et al. Cytokeratin-19 as a biomarker in urine and in serum for the diagnosis of endometriosis-a prospective study. Gynecol Endocrinol 2014, 30:38-41.
11. Wang C., Fang W., Lee C.S. Recent advances in capillary electrophoresis-based proteomic techniques for biomarker discovery. Capillary Electrophoresis of Biomolecules Methods in Molecular Biology 2013, 1-12. Humana Press. N. Volpi, F. Maccari (Eds.).
12. Wolfler M.M., Meinhold-Heerlein I.M., Sohngen L., Rath W., Knuchel R., Neulen J., et al. Two-dimensional gel electrophoresis in peritoneal fluid samples identifies differential protein regulation in patients suffering from peritoneal or ovarian endometriosis. Fertil Steril 2011, 95:2764-2768.
13. Ferrero S., Gillott D.J., Remorgida V., Anserini P., Ragni N., Grudzinskas J.G. GnRH analogue remarkably down-regulates inflammatory proteins in peritoneal fluid proteome of women with endometriosis. J Reprod Med 2009, 54:223-231.
14. Ferrero S., Gillott D.J., Remorgida V., Anserini P., Ragni N., Grudzinskas J.G. Proteomic analysis of peritoneal fluid in fertile and infertile women with endometriosis. J Reprod Med 2009, 54:32-40.
15. Perez-Perez R., Garcia-Santos E., Ortega-Delgado F.J., Lopez J.A., Camafeita E., Ricart W., et al. Attenuated metabolism is a hallmark of obesity as revealed by comparative proteomic analysis of human omental adipose tissue. J Proteomics 2012, 75:783-795.
16. Giudice L.C. Clinical practice. Endometriosis. N Engl J Med 2010, 362:2389-2398.
17. Buck Louis G.M., Hediger M.L., Peterson C.M., Croughan M., Sundaram R., Stanford J., et al. Incidence of endometriosis by study population and diagnostic method: the ENDO study. Fertil Steril 2011, 96:360-365.
18. Sampson J.A. Peritoneal endometriosis due to the menstrual dissemination of endometrial tissue into the peritoneal cavity. Am J Obstet Gynecol 1927, 14:422-469.
19. Halban J. Hysteroadenosis metastica. Wien Klin Wochenschr 1924, 37:1205-1228.
20. Ulukus M., Arici A. Immunology of endometriosis. Minerva Ginecol 2005, 57:237-248.
21. Meyer R. Uber entzundliche neterope epithelwucherungen im weiblichen Genetalg ebiet und uber eine bis in die Wurzel des Nesocolon ausgedehnte benigne Wucherung des Dar mepithel. Virch Arch Pathol Anat 1909, 195:487.
22. Bulun S.E. Endometriosis. N Engl J Med 2009, 360:268-279.
23. Berkley K.J., Rapkin A.J., Papka R.E. The pains of endometriosis. Science 2005, 308:1587-1589.
24. Tokushige N., Markham R., Russell P., Fraser I.S. Nerve fibres in peritoneal endometriosis. Hum Reprod 2006, 21:3001-3007.
25. Diamanti-Kandarakis E., Bourguignon J.P., Giudice L.C., Hauser R., Prins G.S., Soto A.M., et al. Endocrine-disrupting chemicals: an Endocrine Society scientific statement. Endocr Rev 2009, 30:293-342.
26. Pellacani C., Buschini A., Galati S., Mussi F., Franzoni S., Costa L.G. Evaluation of DNA damage induced by 2 polybrominated diphenyl ether flame retardants (BDE-47 and BDE-209) in SK-N-MC cells. Int J Toxicol 2012, 31:372-379.
27. Cobellis L., Latini G., De Felice C., Razzi S., Paris I., Ruggieri F., et al. High plasma concentrations of di-(2-ethylhexyl)-phthalate in women with endometriosis. Hum Reprod 2003, 18:1512-1515.
28. Louis G.M., Weiner J.M., Whitcomb B.W., Sperrazza R., Schisterman E.F., Lobdell D.T., et al. Environmental PCB exposure and risk of endometriosis. Hum Reprod 2005, 20:279-285.
29. Reddy B.S., Rozati R., Reddy B.V., Raman N.V. Association of phthalate esters with endometriosis in Indian women. BJOG 2006, 113:515-520.
30. Signorile P.G., Spugnini E.P., Mita L., Mellone P., D'Avino A., Bianco M., et al. Pre-natal exposure of mice to bisphenol A elicits an endometriosis-like phenotype in female offspring. Gen Comp Endocrinol 2010, 168:318-325.
31. Kim S.H., Chun S., Jang J.Y., Chae H.D., Kim C.H., Kang B.M. Increased plasma levels of phthalate esters in women with advanced-stage endometriosis: a prospective case-control study. Fertil Steril 2011, 95:357-359.
32. Signorile P.G., Spugnini E.P., Citro G., Viceconte R., Vincenzi B., Baldi F., et al. Endocrine disruptors in utero cause ovarian damages linked to endometriosis. Front Biosci (Elite Ed) 2012, 4:1724-1730.
33. Buck Louis G.M., Chen Z., Peterson C.M., Hediger M.L., Croughan M.S., Sundaram R., et al. Persistent lipophilic environmental chemicals and endometriosis: the ENDO Study. Environ Health Perspect 2012, 120:811-816.
34. Buck Louis G.M., Peterson C.M., Chen Z., Croughan M., Sundaram R., Stanford J., et al. Bisphenol A and phthalates and endometriosis: the endometriosis: Natural History, Diagnosis and Outcomes Study. Fertil Steril 2013, 100:162-169. [e1-2].
35. Dowell J.A., Frost D.C., Zhang J., Li L. Comparison of two-dimensional fractionation techniques for shotgun proteomics. Anal Chem 2008, 80:6715-6723.
36. Wang Y., Yang F., Gritsenko M.A., Wang Y., Clauss T., Liu T., et al. Reversed-phase chromatography with multiple fraction concatenation strategy for proteome profiling of human MCF10A cells. Proteomics 2011, 11:2019-2026.
37. Benjamini Y., Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B (Methodol) 1995, 57:289-300.
38. Reich M., Liefeld T., Gould J., Lerner J., Tamayo P., Mesirov J.P. GenePattern 2.0. Nat Genet 2006, 38:500-501.
39. Zhou Y., McMaster M., Woo K., Janatpour M., Perry J., Karpanen T., et al. Vascular endothelial growth factor ligands and receptors that regulate human cytotrophoblast survival are dysregulated in severe preeclampsia and hemolysis, elevated liver enzymes, and low platelets syndrome. Am J Pathol 2002, 160:1405-1423.
40. Johnson-Restrepo B., Kannan K., Rapaport D.P., Rodan B.D. Polybrominated diphenyl ethers and polychlorinated biphenyls in human adipose tissue from New York. Environ Sci Technol 2005, 39:5177-5182.
41. Rudnick P.A., Clauser K.R., Kilpatrick L.E., Tchekhovskoi D.V., Neta P., Blonder N., et al. Performance metrics for liquid chromatography-tandem mass spectrometry systems in proteomics analyses. Mol Cell Proteomics 2010, 9:225-241.
42. Ishihama Y., Oda Y., Tabata T., Sato T., Nagasu T., Rappsilber J., et al. Exponentially modified protein abundance index (emPAI) for estimation of absolute protein amount in proteomics by the number of sequenced peptides per protein. Mol Cell Proteomics 2005, 4:1265-1272.
43. Adachi J., Kumar C., Zhang Y., Olsen J.V., Mann M. The human urinary proteome contains more than 1500 proteins, including a large proportion of membrane proteins. Genome Biol 2006, 7:R80.
44. Rai P., Kota V., Deendayal M., Shivaji S. Differential proteome profiling of eutopic endometrium from women with endometriosis to understand etiology of endometriosis. J Proteome Res 2010, 9:4407-4419.
45. Wolfler M.M., Meinhold-Heerlein I.M., Henkel C., Rath W., Neulen J., Maass N., et al. Reduced hemopexin levels in peritoneal fluid of patients with endometriosis. Fertil Steril 2013, 100:777-781.
46. Ferrero S., Gillott D.J., Remorgida V., Anserini P., Leung K.Y., Ragni N., et al. Proteomic analysis of peritoneal fluid in women with endometriosis. J Proteome Res 2007, 6:3402-3411.
47. Ferrero S., Gillott D.J., Remorgida V., Anserini P., Ragni N., Grudzinskas J.G. Peritoneal fluid proteome in women with different ASRM stages of endometriosis. Gynecol Endocrinol 2008, 24:433-441.
48. El-Kasti M.M., Wright C., Fye H.K., Roseman F., Kessler B.M., Becker C.M. Urinary peptide profiling identifies a panel of putative biomarkers for diagnosing and staging endometriosis. Fertil Steril 2011, 95:1261-1266. [e1-6].
49. Becker C.M., Louis G., Exarhopoulos A., Mechsner S., Ebert A.D., Zurakowski D., et al. Matrix metalloproteinases are elevated in the urine of patients with endometriosis. Fertil Steril 2010, 94:2343-2346.
50. Ngo C., Chereau C., Nicco C., Weill B., Chapron C., Batteux F. Reactive oxygen species controls endometriosis progression. Am J Pathol 2009, 175:225-234.
51. Kao L.C., Germeyer A., Tulac S., Lobo S., Yang J.P., Taylor R.N., et al. Expression profiling of endometrium from women with endometriosis reveals candidate genes for disease-based implantation failure and infertility. Endocrinology 2003, 144:2870-2881.
52. Stephens A.N., Hannan N.J., Rainczuk A., Meehan K.L., Chen J., Nicholls P.K., et al. Post-translational modifications and protein-specific isoforms in endometriosis revealed by 2D DIGE. J Proteome Res 2010, 9:2438-2449.
53. D'Cruz O.J., Wild R.A., Haas G.G., Reichlin M. Antibodies to carbonic anhydrase in endometriosis: prevalence, specificity, and relationship to clinical and laboratory parameters. Fertil Steril 1996, 66:547-556.
54. Hull M.L., Escareno C.R., Godsland J.M., Doig J.R., Johnson C.M., Phillips S.C., et al. Endometrial-peritoneal interactions during endometriotic lesion establishment. Am J Pathol 2008, 173:700-715.
55. Xu Y.L., Wang D.B., Liu Q.F., Chen Y.H., Yang Z. Silencing of cofilin-1 gene attenuates biological behaviours of stromal cells derived from eutopic endometria of women with endometriosis. Hum Reprod 2010, 25:2480-2488.
56. Kats R., Collette T., Metz C.N., Akoum A. Marked elevation of macrophage migration inhibitory factor in the peritoneal fluid of women with endometriosis. Fertil Steril 2002, 78:69-76.
57. Khoufache K., Bazin S., Girard K., Guillemette J., Roy M.C., Verreault J.P., et al. Macrophage migration inhibitory factor antagonist blocks the development of endometriosis in vivo. PLoS One 2012, 7:e37264.
58. Rai P., Shivaji S. The role of DJ-1 in the pathogenesis of endometriosis. PLoS One 2011, 6:e18074.
59. Han S.J., Hawkins S.M., Begum K., Jung S.Y., Kovanci E., Qin J., et al. A new isoform of steroid receptor coactivator-1 is crucial for pathogenic progression of endometriosis. Nat Med 2012, 18:1102-1111.
60. Shimoya K., Moriyama A., Ogata I., Nobunaga T., Koyama M., Azuma C., et al. Increased concentrations of secretory leukocyte protease inhibitor in peritoneal fluid of women with endometriosis. Mol Hum Reprod 2000, 6:829-834.
61. Gilli F., Navone N.D., Perga S., Marnetto F., Caldano M., Capobianco M., et al. Loss of braking signals during inflammation: a factor affecting the development and disease course of multiple sclerosis. Arch Neurol 2011, 68:879-888.