Skip to main content
Top
Published in: Journal of Ovarian Research 1/2014

Open Access 01-12-2014 | Research

Proteomic identification of fucosylated haptoglobin alpha isoforms in ascitic fluids and its localization in ovarian carcinoma tissues from Mexican patients

Authors: Olga Lilia Garibay-Cerdenares, Verónica Ivonne Hernández-Ramírez, Juan Carlos Osorio-Trujillo, Magdalena Hernández-Ortíz, Dolores Gallardo-Rincón, David Cantú de León, Sergio Encarnación-Guevara, Julio César Villegas-Pineda, Patricia Talamás-Rohana

Published in: Journal of Ovarian Research | Issue 1/2014

Login to get access

Abstract

Background

Ovarian cancer is the most lethal gynecologic disease due to delayed diagnosis, and ascites production is a characteristic of patients in advanced stages. The aim of this study was to perform the proteomic analysis of ascitic fluids of Mexican patients with ovarian carcinoma, in order to detect proteins with a differential expression pattern in the continuing search to identify biomarkers for this disease.

Methods

Samples were collected from 50 patients from the Instituto Nacional de Cancerología of México under informed consent and with approval of the bioethics and scientific committees. After elimination of abundant proteins (Albumin/IgGs) samples were processed for 2D electrophoresis and further protein identification by Mass Spectrometry (MALDI-TOF). Molecules of interest were followed by western blot and lectin binding assays, and their tissue location by histo-immunofluorescence and confocal analysis.

Results and discussion

An area with a differential expression pattern among samples was located in the 2D gels. Identified proteins were 6 alpha 1 isoforms and 1 alpha 2 isoform of Haptoglobin, and 2 isoforms of Transthyretin. While Transthyretin isoforms were constitutively expressed in all samples, clear differences in the expression pattern of Haptoglobin alpha isoforms were found. Moreover, increased levels of fucosylation of Haptoglobin alpha isoforms analyzed in 40 samples by Aleuria aurantia lectin binding by 1D overlay assay showed a positive correlation with advanced stages of the disease. Tissue detection of Haptoglobin and its fucosylated form, by histo-immunofluorescence in biopsies of ovarian cancer, also showed a correlation with ovarian cancer progression. Moreover, results show that fucosylated Haptoglobin is produced by tumor cells.

Conclusions

Increased numbers of highly fucosylated Haptoglobin alpha isoforms in ascitic fluids and the presence of fucosylated Haptoglobin in tumor tissues of ovarian cancer Mexican patients associated with advanced stages of the disease, reinforce the potential of fucosylated Haptoglobin alpha isoforms to be characterized as biomarkers for disease progression.
Appendix
Available only for authorised users
Literature
1.
go back to reference Siegel R, Naishadham D, Jemal A: Cancer statistics, 2012. CA Cancer J Clin 2012, 62: 10–29. 10.3322/caac.20138CrossRefPubMed Siegel R, Naishadham D, Jemal A: Cancer statistics, 2012. CA Cancer J Clin 2012, 62: 10–29. 10.3322/caac.20138CrossRefPubMed
2.
go back to reference Kim A, Ueda Y, Naka T, Enomoto T: Therapeutic strategies in epithelial ovarian cancer. BMC Cancer 2012, 31: 14. Kim A, Ueda Y, Naka T, Enomoto T: Therapeutic strategies in epithelial ovarian cancer. BMC Cancer 2012, 31: 14.
3.
go back to reference Lamendola DE, Duan Z, Yusuf RZ, Seiden MV: Molecular description of evolving paclitaxel resistance in the SKOV-3 human ovarian carcinoma cell line. Cancer Res 2003, 63: 2200–2205.PubMed Lamendola DE, Duan Z, Yusuf RZ, Seiden MV: Molecular description of evolving paclitaxel resistance in the SKOV-3 human ovarian carcinoma cell line. Cancer Res 2003, 63: 2200–2205.PubMed
4.
go back to reference Ouellet V, Zietarska M, Portelance L, Lafontaine J, Madore J, Puiffe M-L, Arcand SL, Shen Z, Hébert J, Tonin PN, Provencher DM, Mes-Masson A-M: Characterization of three new serous epithelial ovarian cancer cell lines. BMC Cancer 2008, 8: 152. 10.1186/1471-2407-8-152PubMedCentralCrossRefPubMed Ouellet V, Zietarska M, Portelance L, Lafontaine J, Madore J, Puiffe M-L, Arcand SL, Shen Z, Hébert J, Tonin PN, Provencher DM, Mes-Masson A-M: Characterization of three new serous epithelial ovarian cancer cell lines. BMC Cancer 2008, 8: 152. 10.1186/1471-2407-8-152PubMedCentralCrossRefPubMed
5.
go back to reference Sharrow A, Ronnett B, Thoburn C, Barber J, Giuntoli R, Armstrong D, Jones R, Hess A: Identification and characterization of a spontaneous ovarian carcinoma in Lewis rats. J Ovarian Res 2010, 3: 9. 10.1186/1757-2215-3-9PubMedCentralCrossRefPubMed Sharrow A, Ronnett B, Thoburn C, Barber J, Giuntoli R, Armstrong D, Jones R, Hess A: Identification and characterization of a spontaneous ovarian carcinoma in Lewis rats. J Ovarian Res 2010, 3: 9. 10.1186/1757-2215-3-9PubMedCentralCrossRefPubMed
6.
go back to reference Tan DSP, Agarwal R, Kaye SB: Mechanisms of transcoelomic metastasis in ovarian cancer. Lancet Oncol 2006, 7: 925–934. 10.1016/S1470-2045(06)70939-1CrossRefPubMed Tan DSP, Agarwal R, Kaye SB: Mechanisms of transcoelomic metastasis in ovarian cancer. Lancet Oncol 2006, 7: 925–934. 10.1016/S1470-2045(06)70939-1CrossRefPubMed
7.
go back to reference Amadori D, Sansoni E, Amadori F: Ovarian cancer: natural history and metastatic pattern. Front Biosci 1997, 1: 8–10. Amadori D, Sansoni E, Amadori F: Ovarian cancer: natural history and metastatic pattern. Front Biosci 1997, 1: 8–10.
8.
go back to reference Berchuck A, Carney M: Human ovarian cancer of the surface epithelium. Biochem Pharmacol 1997, 54: 541–544. 10.1016/S0006-2952(97)00061-0CrossRefPubMed Berchuck A, Carney M: Human ovarian cancer of the surface epithelium. Biochem Pharmacol 1997, 54: 541–544. 10.1016/S0006-2952(97)00061-0CrossRefPubMed
9.
go back to reference Davidson B, Espina V, Steinberg SM, Flørenes VA, Liotta LA, Kristensen GB, Tropé CG, Berner A, Kohn EC: Proteomic analysis of malignant ovarian cancer effusions as a tool for biologic and prognostic profiling. Clin Cancer Res 2006, 12: 791–799. 10.1158/1078-0432.CCR-05-2516CrossRefPubMed Davidson B, Espina V, Steinberg SM, Flørenes VA, Liotta LA, Kristensen GB, Tropé CG, Berner A, Kohn EC: Proteomic analysis of malignant ovarian cancer effusions as a tool for biologic and prognostic profiling. Clin Cancer Res 2006, 12: 791–799. 10.1158/1078-0432.CCR-05-2516CrossRefPubMed
10.
go back to reference Qian W, Jacobs J, Liu T, Camp D, Smith R: Advances and challenges in liquid chromatography-mass spectrometry-based proteomics profiling for clinical applications. Mol Cell Proteomics 2006, 5: 1727–1744. 10.1074/mcp.M600162-MCP200PubMedCentralCrossRefPubMed Qian W, Jacobs J, Liu T, Camp D, Smith R: Advances and challenges in liquid chromatography-mass spectrometry-based proteomics profiling for clinical applications. Mol Cell Proteomics 2006, 5: 1727–1744. 10.1074/mcp.M600162-MCP200PubMedCentralCrossRefPubMed
11.
go back to reference Huang H, Li Y, Liu J, Zheng M, Feng Y, Hu K, Huang Y, Huang Q: Screening and identification of biomarkers in ascites related to intrinsic chemoresistance of serous epithelial ovarian cancers. PLoS One 2012, 12: e51256.CrossRef Huang H, Li Y, Liu J, Zheng M, Feng Y, Hu K, Huang Y, Huang Q: Screening and identification of biomarkers in ascites related to intrinsic chemoresistance of serous epithelial ovarian cancers. PLoS One 2012, 12: e51256.CrossRef
12.
go back to reference Sundfeldt K, Ivarsson K, Rask K, Haeger M, Hedin L, Brännström M: Higher levels of soluble E-cadherin in cyst fluid from malignant ovarian tumours than in benign cysts. Anticancer Res 2001, 21: 65–70.PubMed Sundfeldt K, Ivarsson K, Rask K, Haeger M, Hedin L, Brännström M: Higher levels of soluble E-cadherin in cyst fluid from malignant ovarian tumours than in benign cysts. Anticancer Res 2001, 21: 65–70.PubMed
13.
go back to reference Ivarsson K, Runesson E, Sundfeldt K, Haeger M, Hedin L, Janson PO, Brannstrom M: The chemotactic cytokine interleukin-8-a cyst fluid marker for malignant epithelial ovarian cancer? Gynecol Oncol 1998, 71: 420–423. 10.1006/gyno.1998.5198CrossRefPubMed Ivarsson K, Runesson E, Sundfeldt K, Haeger M, Hedin L, Janson PO, Brannstrom M: The chemotactic cytokine interleukin-8-a cyst fluid marker for malignant epithelial ovarian cancer? Gynecol Oncol 1998, 71: 420–423. 10.1006/gyno.1998.5198CrossRefPubMed
14.
go back to reference McIntosh MW, Drescher C, Karlan B, Scholler N, Urban N, Hellstrom KE, Hellstrom I: Combining CA 125 and SMR serum markers for diagnosis and early detection of ovarian carcinoma. Gynecol Oncol 2004, 95: 9–15. 10.1016/j.ygyno.2004.07.039PubMedCentralCrossRefPubMed McIntosh MW, Drescher C, Karlan B, Scholler N, Urban N, Hellstrom KE, Hellstrom I: Combining CA 125 and SMR serum markers for diagnosis and early detection of ovarian carcinoma. Gynecol Oncol 2004, 95: 9–15. 10.1016/j.ygyno.2004.07.039PubMedCentralCrossRefPubMed
15.
go back to reference Seeber B, Sammel MD, Fan X, Gerton GL, Shaunik A, Chittams J, Barnhart KT: Panel of markers can accurately predict endometriosis in a subset of patients. Fertil Steril 2008, 89: 1073–1081. 10.1016/j.fertnstert.2007.05.014CrossRefPubMed Seeber B, Sammel MD, Fan X, Gerton GL, Shaunik A, Chittams J, Barnhart KT: Panel of markers can accurately predict endometriosis in a subset of patients. Fertil Steril 2008, 89: 1073–1081. 10.1016/j.fertnstert.2007.05.014CrossRefPubMed
16.
go back to reference Petri AL, Simonsen AH, Yip T-T, Hogdall E, Fung ET, Lundvall L, Hogdall C: Three new potential ovarian cancer biomarkers detected in human urine with equalizer bead technology. Acta Obst Gynecol Scand 2009, 88: 18–26. 10.1080/00016340802443830CrossRef Petri AL, Simonsen AH, Yip T-T, Hogdall E, Fung ET, Lundvall L, Hogdall C: Three new potential ovarian cancer biomarkers detected in human urine with equalizer bead technology. Acta Obst Gynecol Scand 2009, 88: 18–26. 10.1080/00016340802443830CrossRef
17.
go back to reference Waldemarson S, Krogh M, Alaiya A, Kirik U, Schedvins K, Auer G, Hansson KM, Ossola R, Aebersold R, Lee H, Malmstrom J, James P: Protein expression changes in ovarian cancer during the transition from benign to malignant. J Proteome Res 2012, 11: 2876–2889. 10.1021/pr201258qCrossRefPubMed Waldemarson S, Krogh M, Alaiya A, Kirik U, Schedvins K, Auer G, Hansson KM, Ossola R, Aebersold R, Lee H, Malmstrom J, James P: Protein expression changes in ovarian cancer during the transition from benign to malignant. J Proteome Res 2012, 11: 2876–2889. 10.1021/pr201258qCrossRefPubMed
18.
go back to reference Peterson V, Castro C, Chung J, Miller N, Ullal A, Castano M, Penson R, Lee H, Birrer M, Weissleder R: Ascites analysis by a microfluidic chip allows tumor-cell profiling. Proc Natl Acad Sci 2013, 110: E4978-E4986. 10.1073/pnas.1315370110PubMedCentralCrossRefPubMed Peterson V, Castro C, Chung J, Miller N, Ullal A, Castano M, Penson R, Lee H, Birrer M, Weissleder R: Ascites analysis by a microfluidic chip allows tumor-cell profiling. Proc Natl Acad Sci 2013, 110: E4978-E4986. 10.1073/pnas.1315370110PubMedCentralCrossRefPubMed
19.
go back to reference Benedet L, Bender H, III HJ, Ngan HY, Pecorelli S: FIGO staging classifications and clinical practice guidelines in the management of gynecologic cancers. FIGO committee on gynecologic oncology. Int J Gynaecol Obstet 2000, 70: 209–262.CrossRefPubMed Benedet L, Bender H, III HJ, Ngan HY, Pecorelli S: FIGO staging classifications and clinical practice guidelines in the management of gynecologic cancers. FIGO committee on gynecologic oncology. Int J Gynaecol Obstet 2000, 70: 209–262.CrossRefPubMed
20.
go back to reference Klose J, Kobalz U: Two-dimensional electrophoresis of proteins: an updated protocol and implications for a functional analysis of the genome. Electrophoresis 1995, 16: 1034–1059. 10.1002/elps.11501601175CrossRefPubMed Klose J, Kobalz U: Two-dimensional electrophoresis of proteins: an updated protocol and implications for a functional analysis of the genome. Electrophoresis 1995, 16: 1034–1059. 10.1002/elps.11501601175CrossRefPubMed
21.
go back to reference Higareda-Almaraz JC, Enríquez-Gasca MR, Hernández-Ortiz M, Resendis-Antonio O, Encarnación-Guevara S: Proteomic patterns of cervical cancer cell lines, a network perspective. BMC Syst Biol 2011, 5: 96. 10.1186/1752-0509-5-96PubMedCentralCrossRefPubMed Higareda-Almaraz JC, Enríquez-Gasca MR, Hernández-Ortiz M, Resendis-Antonio O, Encarnación-Guevara S: Proteomic patterns of cervical cancer cell lines, a network perspective. BMC Syst Biol 2011, 5: 96. 10.1186/1752-0509-5-96PubMedCentralCrossRefPubMed
22.
go back to reference Kochibe N, Furukawa K: Purification and properties of a novel fucose-specific hemagglutinin of Aleuria aurantia . Biochemistry 1980, 19: 2841–2846. 10.1021/bi00554a004CrossRefPubMed Kochibe N, Furukawa K: Purification and properties of a novel fucose-specific hemagglutinin of Aleuria aurantia . Biochemistry 1980, 19: 2841–2846. 10.1021/bi00554a004CrossRefPubMed
23.
go back to reference Black JA, Dixon GH: Amino-acid sequence of alpha chains of human haptoglobins. Nature 1968, 218: 736–741. 10.1038/218736a0CrossRefPubMed Black JA, Dixon GH: Amino-acid sequence of alpha chains of human haptoglobins. Nature 1968, 218: 736–741. 10.1038/218736a0CrossRefPubMed
24.
go back to reference Fish RG, Gill TS, Adams M, Kerby I: Serum haptoglobin and α1-acid glycoprotein as indicators of the effectiveness of cis-diamminedichloroplatinum (CDDP) in ovarian cancer patients—a preliminary report. Eur J Cancer Clin Oncol 1984, 20: 625–630. 10.1016/0277-5379(84)90007-5CrossRefPubMed Fish RG, Gill TS, Adams M, Kerby I: Serum haptoglobin and α1-acid glycoprotein as indicators of the effectiveness of cis-diamminedichloroplatinum (CDDP) in ovarian cancer patients—a preliminary report. Eur J Cancer Clin Oncol 1984, 20: 625–630. 10.1016/0277-5379(84)90007-5CrossRefPubMed
25.
go back to reference Park S-J, Baek SH, Oh M-K, Choi SH, Park EH, Kim N-H, Shin J-C, Kim I-S: Enhancement of angiogenic and vasculogenic potential of endothelial progenitor cells by haptoglobin. FEBS Lett 2009, 583: 3235–3240. 10.1016/j.febslet.2009.09.014CrossRefPubMed Park S-J, Baek SH, Oh M-K, Choi SH, Park EH, Kim N-H, Shin J-C, Kim I-S: Enhancement of angiogenic and vasculogenic potential of endothelial progenitor cells by haptoglobin. FEBS Lett 2009, 583: 3235–3240. 10.1016/j.febslet.2009.09.014CrossRefPubMed
26.
go back to reference Narisada M, Kawamoto S, Kuwamoto K, Moriwaki K, Nakagawa T, Matsumoto H, Asahi M, Koyama N, Miyoshi E: Identification of an inducible factor secreted by pancreatic cancer cell lines that stimulates the production of fucosylated haptoglobin in hepatoma cells. Biochem Biophys Res Commun 2008, 377: 792–796. 10.1016/j.bbrc.2008.10.061CrossRefPubMed Narisada M, Kawamoto S, Kuwamoto K, Moriwaki K, Nakagawa T, Matsumoto H, Asahi M, Koyama N, Miyoshi E: Identification of an inducible factor secreted by pancreatic cancer cell lines that stimulates the production of fucosylated haptoglobin in hepatoma cells. Biochem Biophys Res Commun 2008, 377: 792–796. 10.1016/j.bbrc.2008.10.061CrossRefPubMed
27.
go back to reference Okuyama N, Ide Y, Nakano M, Nakagawa T, Yamanaka K, Moriwaki K, Murata K, Ohigashi H, Yokoyama S, Eguchi H, Ishikawa O, Ito T, Kato M, Kasahara A, Kawano S, Gu J, Taniguchi N, Miyoshi E: Fucosylated haptoglobin is a novel marker for pancreatic cancer: a detailed analysis of the oligosaccharide structure and a possible mechanism for fucosylation. Int J Cancer 2006, 118: 2803–2808. 10.1002/ijc.21728CrossRefPubMed Okuyama N, Ide Y, Nakano M, Nakagawa T, Yamanaka K, Moriwaki K, Murata K, Ohigashi H, Yokoyama S, Eguchi H, Ishikawa O, Ito T, Kato M, Kasahara A, Kawano S, Gu J, Taniguchi N, Miyoshi E: Fucosylated haptoglobin is a novel marker for pancreatic cancer: a detailed analysis of the oligosaccharide structure and a possible mechanism for fucosylation. Int J Cancer 2006, 118: 2803–2808. 10.1002/ijc.21728CrossRefPubMed
28.
go back to reference Markman M: The role of CA-125 in the management of ovarian cancer. Oncologist 1997, 2: 6–9.PubMed Markman M: The role of CA-125 in the management of ovarian cancer. Oncologist 1997, 2: 6–9.PubMed
29.
go back to reference Terry K, Sluss P, Skates S, Mok S, Ye B, Vitonis A, Cramer D: Blood and urine markers for ovarian cancer: a comprehensive review. Dis Markers 2004, 20: 53–70. 10.1155/2004/241982PubMedCentralCrossRefPubMed Terry K, Sluss P, Skates S, Mok S, Ye B, Vitonis A, Cramer D: Blood and urine markers for ovarian cancer: a comprehensive review. Dis Markers 2004, 20: 53–70. 10.1155/2004/241982PubMedCentralCrossRefPubMed
30.
go back to reference Drapkin R, von Horsten HH, Lin Y, Mok SC, Crum CP, Welch WR, Hecht JL: Human epididymis protein 4 (HE4) is a secreted glycoprotein that is overexpressed by serous and endometrioid ovarian carcinomas. Cancer Res 2005, 65: 2162–2169. 10.1158/0008-5472.CAN-04-3924CrossRefPubMed Drapkin R, von Horsten HH, Lin Y, Mok SC, Crum CP, Welch WR, Hecht JL: Human epididymis protein 4 (HE4) is a secreted glycoprotein that is overexpressed by serous and endometrioid ovarian carcinomas. Cancer Res 2005, 65: 2162–2169. 10.1158/0008-5472.CAN-04-3924CrossRefPubMed
31.
go back to reference Huhtinen K, Suvitie P, Hiissa J, Junnila J, Huvila J, Kujari H, Setälä M, Härkki P, Jalkanen J, Fraser J, Mäkinen J, Auranen A, Poutanen M, Perheentupa A: Serum HE4 concentration differentiates malignant ovarian tumours from ovarian endometriotic cysts. Br J Cancer 2009, 100: 1315–1319. 10.1038/sj.bjc.6605011PubMedCentralCrossRefPubMed Huhtinen K, Suvitie P, Hiissa J, Junnila J, Huvila J, Kujari H, Setälä M, Härkki P, Jalkanen J, Fraser J, Mäkinen J, Auranen A, Poutanen M, Perheentupa A: Serum HE4 concentration differentiates malignant ovarian tumours from ovarian endometriotic cysts. Br J Cancer 2009, 100: 1315–1319. 10.1038/sj.bjc.6605011PubMedCentralCrossRefPubMed
32.
go back to reference Schweigert F, Wirth K, Raila J: Characterization of the microheterogeneity of transthyretin in plasma and urine using SELDI-TOF-MS immunoassay. Proteome Sci 2004, 2: 5. 10.1186/1477-5956-2-5PubMedCentralCrossRefPubMed Schweigert F, Wirth K, Raila J: Characterization of the microheterogeneity of transthyretin in plasma and urine using SELDI-TOF-MS immunoassay. Proteome Sci 2004, 2: 5. 10.1186/1477-5956-2-5PubMedCentralCrossRefPubMed
33.
go back to reference Su F, Kozak K, Imaizumi S, Gao F, Amneus M, Grijalva V, Ng C, Wagner A, Hough G, Farias-Eisner G, Anantharamaiah G, Lenten BV, Navab M, Fogelman A, Reddy S, Farias-Eisner R: Apolipoprotein A-I (apoA-I) and apoA-I mimetic peptides inhibit tumor development in a mouse model of ovarian cancer. Proc Natl Acad Sci 2010, 107: 19997–20002. 10.1073/pnas.1009010107PubMedCentralCrossRefPubMed Su F, Kozak K, Imaizumi S, Gao F, Amneus M, Grijalva V, Ng C, Wagner A, Hough G, Farias-Eisner G, Anantharamaiah G, Lenten BV, Navab M, Fogelman A, Reddy S, Farias-Eisner R: Apolipoprotein A-I (apoA-I) and apoA-I mimetic peptides inhibit tumor development in a mouse model of ovarian cancer. Proc Natl Acad Sci 2010, 107: 19997–20002. 10.1073/pnas.1009010107PubMedCentralCrossRefPubMed
34.
go back to reference Lokshin AE, Winans M, Landsittel D, Marrangoni AM, Velikokhatnaya L, Modugno F, Nolen BM, Gorelik E: Circulating IL-8 and anti-IL-8 autoantibody in patients with ovarian cancer. Gynecol Oncol 2006, 102: 244–251. 10.1016/j.ygyno.2005.12.011CrossRefPubMed Lokshin AE, Winans M, Landsittel D, Marrangoni AM, Velikokhatnaya L, Modugno F, Nolen BM, Gorelik E: Circulating IL-8 and anti-IL-8 autoantibody in patients with ovarian cancer. Gynecol Oncol 2006, 102: 244–251. 10.1016/j.ygyno.2005.12.011CrossRefPubMed
35.
go back to reference Moshkovskii SA, Vlasova MA, Pyatnitskiy MA, Tikhonova OV, Safarova MR, Makarov OV, Archakov AI: Acute phase serum amyloid A in ovarian cancer as an important component of proteome diagnostic profiling. Proteomics Clin Appl 2007, 1: 107–117. 10.1002/prca.200600229CrossRefPubMed Moshkovskii SA, Vlasova MA, Pyatnitskiy MA, Tikhonova OV, Safarova MR, Makarov OV, Archakov AI: Acute phase serum amyloid A in ovarian cancer as an important component of proteome diagnostic profiling. Proteomics Clin Appl 2007, 1: 107–117. 10.1002/prca.200600229CrossRefPubMed
36.
go back to reference Nguyen L, Cardenas-Goicoechea SJ, Gordon P, Curtin C, Momeni M, Chuang L, Fishman D: Biomarkers for early detection of ovarian cancer. Women’s Health 2013, 9: 171–187. 10.2217/whe.13.2CrossRefPubMed Nguyen L, Cardenas-Goicoechea SJ, Gordon P, Curtin C, Momeni M, Chuang L, Fishman D: Biomarkers for early detection of ovarian cancer. Women’s Health 2013, 9: 171–187. 10.2217/whe.13.2CrossRefPubMed
38.
go back to reference Raynes JG, Eagling S, McAdam KP: Acute-phase protein synthesis in human hepatoma cells: differential regulation of serum amyloid A (SAA) and haptoglobin by interleukin-1 and interleukin-6. Clin Exp Immunol 1991, 83: 488–491.PubMedCentralCrossRefPubMed Raynes JG, Eagling S, McAdam KP: Acute-phase protein synthesis in human hepatoma cells: differential regulation of serum amyloid A (SAA) and haptoglobin by interleukin-1 and interleukin-6. Clin Exp Immunol 1991, 83: 488–491.PubMedCentralCrossRefPubMed
39.
go back to reference Lim YK, Jenner A, Ali AB, Wang Y, Hsu SIH, Chong SM, Baumman H, Halliwell B, Lim S-K: Haptoglobin reduces renal oxidative DNA and tissue damage during phenylhydrazine-induced hemolysis. Kidney Int 2000, 58: 1033–1044. 10.1046/j.1523-1755.2000.00261.xCrossRefPubMed Lim YK, Jenner A, Ali AB, Wang Y, Hsu SIH, Chong SM, Baumman H, Halliwell B, Lim S-K: Haptoglobin reduces renal oxidative DNA and tissue damage during phenylhydrazine-induced hemolysis. Kidney Int 2000, 58: 1033–1044. 10.1046/j.1523-1755.2000.00261.xCrossRefPubMed
40.
go back to reference Cid MC, Grant DS, Hoffman GS, Auerbach R, Fauci AS, Kleinman HK: Identification of haptoglobin as an angiogenic factor in sera from patients with systemic vasculitis. J Clin Invest 1993, 91: 977–985. 10.1172/JCI116319PubMedCentralCrossRefPubMed Cid MC, Grant DS, Hoffman GS, Auerbach R, Fauci AS, Kleinman HK: Identification of haptoglobin as an angiogenic factor in sera from patients with systemic vasculitis. J Clin Invest 1993, 91: 977–985. 10.1172/JCI116319PubMedCentralCrossRefPubMed
41.
go back to reference Lohr NL, Warltier DC, Chilian WM, Weihrauch D: Haptoglobin expression and activity during coronary collateralization. Am J Physiol Heart Circ Physiol 2005, 288: H1389-H1395.CrossRefPubMed Lohr NL, Warltier DC, Chilian WM, Weihrauch D: Haptoglobin expression and activity during coronary collateralization. Am J Physiol Heart Circ Physiol 2005, 288: H1389-H1395.CrossRefPubMed
42.
go back to reference Smeets MB, Pasterkamp G, Lim S-K, Velema E, van Middelaar B, de Kleijn DPV: Nitric oxide synthesis is involved in arterial haptoglobin expression after sustained flow changes. FEBS Lett 2002, 529: 221–224. 10.1016/S0014-5793(02)03343-4CrossRefPubMed Smeets MB, Pasterkamp G, Lim S-K, Velema E, van Middelaar B, de Kleijn DPV: Nitric oxide synthesis is involved in arterial haptoglobin expression after sustained flow changes. FEBS Lett 2002, 529: 221–224. 10.1016/S0014-5793(02)03343-4CrossRefPubMed
43.
go back to reference Ahmed N, Barker G, Oliva KT, Hoffmann P, Riley C, Reeve S, Smith AL, Kemp BE, Quinn MA, Rice GE: Proteomic-based identification of haptoglobin-1 precursor as a novel circulating biomarker of ovarian cancer. Br J Cancer 2004, 91: 129–140. 10.1038/sj.bjc.6601882PubMedCentralCrossRefPubMed Ahmed N, Barker G, Oliva KT, Hoffmann P, Riley C, Reeve S, Smith AL, Kemp BE, Quinn MA, Rice GE: Proteomic-based identification of haptoglobin-1 precursor as a novel circulating biomarker of ovarian cancer. Br J Cancer 2004, 91: 129–140. 10.1038/sj.bjc.6601882PubMedCentralCrossRefPubMed
44.
go back to reference Faça VM, Hanash SM: In-depth proteomics to define the cell surface and secretome of ovarian cancer cells and processes of protein shedding. Cancer Res 2009, 69: 728–730. 10.1158/0008-5472.CAN-08-3087CrossRefPubMed Faça VM, Hanash SM: In-depth proteomics to define the cell surface and secretome of ovarian cancer cells and processes of protein shedding. Cancer Res 2009, 69: 728–730. 10.1158/0008-5472.CAN-08-3087CrossRefPubMed
45.
go back to reference Mueller W, Handschumacher R, Wade M: Serum haptoglobin in patients with ovarian malignancies. Obstet Gynecol 1971, 38: 427–435.PubMed Mueller W, Handschumacher R, Wade M: Serum haptoglobin in patients with ovarian malignancies. Obstet Gynecol 1971, 38: 427–435.PubMed
46.
go back to reference Thompson S, Dargan E, Turner G: Increased fucosylation and other carbohydrate changes in haptoglobin in ovarian cancer. Cancer Lett 1992, 14: 43–48.CrossRef Thompson S, Dargan E, Turner G: Increased fucosylation and other carbohydrate changes in haptoglobin in ovarian cancer. Cancer Lett 1992, 14: 43–48.CrossRef
47.
go back to reference Zhao J, Qiu W, Simeone DM, Lubman DM: N-linked glycosylation profiling of pancreatic cancer serum using capillary liquid phase separation coupled with mass spectrometric analysis. J Proteome Res 2007, 6: 1126–1138. 10.1021/pr0604458CrossRefPubMed Zhao J, Qiu W, Simeone DM, Lubman DM: N-linked glycosylation profiling of pancreatic cancer serum using capillary liquid phase separation coupled with mass spectrometric analysis. J Proteome Res 2007, 6: 1126–1138. 10.1021/pr0604458CrossRefPubMed
48.
go back to reference Muinelo-Romay L, Villar-Portela S, Cuevas E, Gil-Martin E, Fernandez-Briera A: Identification of alpha(1,6)fucosylated proteins differentially expressed in human colorectal cancer. BMC Cancer 2011, 11: 508. 10.1186/1471-2407-11-508PubMedCentralCrossRefPubMed Muinelo-Romay L, Villar-Portela S, Cuevas E, Gil-Martin E, Fernandez-Briera A: Identification of alpha(1,6)fucosylated proteins differentially expressed in human colorectal cancer. BMC Cancer 2011, 11: 508. 10.1186/1471-2407-11-508PubMedCentralCrossRefPubMed
50.
go back to reference Kim HJ, Kim SC, Ju W, Kim YH, Yin SY, Kim HJ: Aberrant sialylation and fucosylation of intracellular proteins in cervical tissue are critical markers of cervical carcinogenesis. Oncol Rep 2014, 31: 1417–22.PubMed Kim HJ, Kim SC, Ju W, Kim YH, Yin SY, Kim HJ: Aberrant sialylation and fucosylation of intracellular proteins in cervical tissue are critical markers of cervical carcinogenesis. Oncol Rep 2014, 31: 1417–22.PubMed
51.
go back to reference Dargan E, Thompson S, Cantwell BMJ, Wilson RG, Turner GA: Changes in the fucose content of haptoglobin in breast and ovarian cancer: association with disease progression. Glycoconj J 1994, 1: 37–43. 10.1007/BF00917467 Dargan E, Thompson S, Cantwell BMJ, Wilson RG, Turner GA: Changes in the fucose content of haptoglobin in breast and ovarian cancer: association with disease progression. Glycoconj J 1994, 1: 37–43. 10.1007/BF00917467
52.
go back to reference Yuan K, Listinsky C, Singh R, Listinsky J, Siegal G: Cell surface associated alpha-l-fucose moieties modulate human breast cancer neoplastic progression. Pathol Oncol Res 2008, 14: 145–156. 10.1007/s12253-008-9036-xCrossRefPubMed Yuan K, Listinsky C, Singh R, Listinsky J, Siegal G: Cell surface associated alpha-l-fucose moieties modulate human breast cancer neoplastic progression. Pathol Oncol Res 2008, 14: 145–156. 10.1007/s12253-008-9036-xCrossRefPubMed
53.
go back to reference Wu J, Xie X, Liu Y, He J, Benitez R, Buckanovich RJ, Lubman DM: Identification and confirmation of differentially expressed fucosylated glycoproteins in the serum of ovarian cancer patients using a lectin array and LC-MS/MS. J Proteome Res 2006, 11: 4541–4552.CrossRef Wu J, Xie X, Liu Y, He J, Benitez R, Buckanovich RJ, Lubman DM: Identification and confirmation of differentially expressed fucosylated glycoproteins in the serum of ovarian cancer patients using a lectin array and LC-MS/MS. J Proteome Res 2006, 11: 4541–4552.CrossRef
54.
go back to reference Nabli H, Tuller E, Sharpe-Timms KL: Haptoglobin expression in endometrioid adenocarcinoma of the uterus. Reprod Sci 2010, 17: 47–55. 10.1177/1933719109346331CrossRefPubMed Nabli H, Tuller E, Sharpe-Timms KL: Haptoglobin expression in endometrioid adenocarcinoma of the uterus. Reprod Sci 2010, 17: 47–55. 10.1177/1933719109346331CrossRefPubMed
55.
go back to reference O’Bryan MK, Grima J, Mruk D, Cheng CY: Haptoglobin is a sertoli cell product in the rat seminiferous epithelium: its purification and regulation. J Androl 1997, 18: 637–645.PubMed O’Bryan MK, Grima J, Mruk D, Cheng CY: Haptoglobin is a sertoli cell product in the rat seminiferous epithelium: its purification and regulation. J Androl 1997, 18: 637–645.PubMed
56.
go back to reference Friedrichs WE, Navarijoashbaugh AL, Bowman BH, Yang F: Expression and inflammatory regulation of haptoglobin gene in adipocytes. Biochem Biophys Res Commun 1995, 209: 250–256. 10.1006/bbrc.1995.1496CrossRefPubMed Friedrichs WE, Navarijoashbaugh AL, Bowman BH, Yang F: Expression and inflammatory regulation of haptoglobin gene in adipocytes. Biochem Biophys Res Commun 1995, 209: 250–256. 10.1006/bbrc.1995.1496CrossRefPubMed
57.
go back to reference Olson GE, Winfrey VP, Matrisian PE, Melner MH, Hoffman LH: Specific expression of haptoglobin mRNA in implantation-stage rabbit uterine epithelium. J Endocrinol 1997, 152: 69–80. 10.1677/joe.0.1520069CrossRefPubMed Olson GE, Winfrey VP, Matrisian PE, Melner MH, Hoffman LH: Specific expression of haptoglobin mRNA in implantation-stage rabbit uterine epithelium. J Endocrinol 1997, 152: 69–80. 10.1677/joe.0.1520069CrossRefPubMed
58.
go back to reference Berkova N, Lemay A, Dresser DW, Fontaine J-Y, Kerizit J, Goupil S: Haptoglobin is present in human endometrium and shows elevated levels in the decidua during pregnancy. Mol Hum Reprod 2001, 7: 747–754. 10.1093/molehr/7.8.747CrossRefPubMed Berkova N, Lemay A, Dresser DW, Fontaine J-Y, Kerizit J, Goupil S: Haptoglobin is present in human endometrium and shows elevated levels in the decidua during pregnancy. Mol Hum Reprod 2001, 7: 747–754. 10.1093/molehr/7.8.747CrossRefPubMed
59.
go back to reference Ambekar AS, Nirujogi RS, Srikanth SM, Chavan S, Kelkar DS, Hinduja I, Zaveri K, Prasad TSK, Harsha HC, Pandey A, Mukherjee S: Proteomic analysis of human follicular fluid: a new perspective towards understanding folliculogenesis. J Proteomics 2013, 87: 68–77.CrossRefPubMed Ambekar AS, Nirujogi RS, Srikanth SM, Chavan S, Kelkar DS, Hinduja I, Zaveri K, Prasad TSK, Harsha HC, Pandey A, Mukherjee S: Proteomic analysis of human follicular fluid: a new perspective towards understanding folliculogenesis. J Proteomics 2013, 87: 68–77.CrossRefPubMed
60.
go back to reference D’Armiento J, Dalal SS, Chada K: Tissue, temporal and inducible expression pattern of haptoglobin in mice. Gene 1997, 195: 19–27. 10.1016/S0378-1119(97)00123-6CrossRefPubMed D’Armiento J, Dalal SS, Chada K: Tissue, temporal and inducible expression pattern of haptoglobin in mice. Gene 1997, 195: 19–27. 10.1016/S0378-1119(97)00123-6CrossRefPubMed
61.
go back to reference Benkmann H, Hanssen H, Ovenbeck R, HW HG: Distribution of alpha-1-antitrypsin and haptoglobin phenotypes in bladder cancer patients. Hum Hered 1987, 37: 290–293. 10.1159/000153720CrossRefPubMed Benkmann H, Hanssen H, Ovenbeck R, HW HG: Distribution of alpha-1-antitrypsin and haptoglobin phenotypes in bladder cancer patients. Hum Hered 1987, 37: 290–293. 10.1159/000153720CrossRefPubMed
62.
go back to reference Mitchell R, Carzino R, Janardhana V: Associations between the two serum proteins haptoglobin and transferrin and leukaemia. Hum Hered 1988, 38: 144–150. 10.1159/000153775CrossRefPubMed Mitchell R, Carzino R, Janardhana V: Associations between the two serum proteins haptoglobin and transferrin and leukaemia. Hum Hered 1988, 38: 144–150. 10.1159/000153775CrossRefPubMed
63.
go back to reference Awadallah SM, Atoum MF: Haptoglobin polymorphism in breast cancer patients form Jordan. Clin Chim Acta 2004, 341: 17–21. 10.1016/j.cccn.2003.10.032CrossRefPubMed Awadallah SM, Atoum MF: Haptoglobin polymorphism in breast cancer patients form Jordan. Clin Chim Acta 2004, 341: 17–21. 10.1016/j.cccn.2003.10.032CrossRefPubMed
64.
go back to reference Epelbaum R, Shalitin C, Segal R, Valansi C, Arselan I, Faraggi D, Leviov M, Ben M, Shahar M, Haim N: Haptoglobin-related protein as a serum marker in malignant lymphoma. Pathol Oncol Res 1998, 4: 271–276. 10.1007/BF02905217CrossRefPubMed Epelbaum R, Shalitin C, Segal R, Valansi C, Arselan I, Faraggi D, Leviov M, Ben M, Shahar M, Haim N: Haptoglobin-related protein as a serum marker in malignant lymphoma. Pathol Oncol Res 1998, 4: 271–276. 10.1007/BF02905217CrossRefPubMed
65.
go back to reference Dunzendorfer U, Jung K, Go G: Haptoglobin-related protein as a serum marker in malignant lymphoma. Eur Urol 1980, 6: 232–236.PubMed Dunzendorfer U, Jung K, Go G: Haptoglobin-related protein as a serum marker in malignant lymphoma. Eur Urol 1980, 6: 232–236.PubMed
66.
go back to reference Dunzendorfer U, Jung K, Ohlenschläger G: Transferrin, C3 complement, haptoglobin, plasminogen and alpha 2-microglobulin in patients with urogenital tumors. Eur Urol 1980, 6: 232–236.PubMed Dunzendorfer U, Jung K, Ohlenschläger G: Transferrin, C3 complement, haptoglobin, plasminogen and alpha 2-microglobulin in patients with urogenital tumors. Eur Urol 1980, 6: 232–236.PubMed
67.
go back to reference An J-Y, Fan Z-M, Zhuang Z-H, Qin Y-R, Gao S-S, Li J-L, Wang L-D: Proteomic analysis of blood level of proteins before and after operation in patients with esophageal squamous cell carcinoma at high-incidence area in Henan Province. World J Gastroenterol 2004, 15: 3365–3368.CrossRef An J-Y, Fan Z-M, Zhuang Z-H, Qin Y-R, Gao S-S, Li J-L, Wang L-D: Proteomic analysis of blood level of proteins before and after operation in patients with esophageal squamous cell carcinoma at high-incidence area in Henan Province. World J Gastroenterol 2004, 15: 3365–3368.CrossRef
68.
go back to reference Elg S, Carson L, Fowler J, Twiggs L, Moradi M, Ramakrishnan S: Ascites levels of haptoglobin in patients with ovarian cancer. Cancer 1993, 71: 3938–3941. 10.1002/1097-0142(19930615)71:12<3938::AID-CNCR2820711223>3.0.CO;2-QCrossRefPubMed Elg S, Carson L, Fowler J, Twiggs L, Moradi M, Ramakrishnan S: Ascites levels of haptoglobin in patients with ovarian cancer. Cancer 1993, 71: 3938–3941. 10.1002/1097-0142(19930615)71:12<3938::AID-CNCR2820711223>3.0.CO;2-QCrossRefPubMed
69.
go back to reference Matsumoto H, Shinzaki S, Narisada M, Kawamoto S, Kuwamoto K, Moriwaki K, Kanke F, Satomura S, Kumada T, Miyoshi E: Clinical application of a lectin-antibody ELISA to measure fucosylated haptoglobin in sera of patients with pancreatic cancer. Clin Chem Lab Med 2010, 48: 505–512.CrossRefPubMed Matsumoto H, Shinzaki S, Narisada M, Kawamoto S, Kuwamoto K, Moriwaki K, Kanke F, Satomura S, Kumada T, Miyoshi E: Clinical application of a lectin-antibody ELISA to measure fucosylated haptoglobin in sera of patients with pancreatic cancer. Clin Chem Lab Med 2010, 48: 505–512.CrossRefPubMed
Metadata
Title
Proteomic identification of fucosylated haptoglobin alpha isoforms in ascitic fluids and its localization in ovarian carcinoma tissues from Mexican patients
Authors
Olga Lilia Garibay-Cerdenares
Verónica Ivonne Hernández-Ramírez
Juan Carlos Osorio-Trujillo
Magdalena Hernández-Ortíz
Dolores Gallardo-Rincón
David Cantú de León
Sergio Encarnación-Guevara
Julio César Villegas-Pineda
Patricia Talamás-Rohana
Publication date
01-12-2014
Publisher
BioMed Central
Published in
Journal of Ovarian Research / Issue 1/2014
Electronic ISSN: 1757-2215
DOI
https://doi.org/10.1186/1757-2215-7-27

Other articles of this Issue 1/2014

Journal of Ovarian Research 1/2014 Go to the issue