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Published in: Reproductive Biology and Endocrinology 1/2013

Open Access 01-12-2013 | Research

Proteomic analysis of human spermatozoa proteins with oxidative stress

Authors: Rakesh Sharma, Ashok Agarwal, Gayatri Mohanty, Alaa J Hamada, Banu Gopalan, Belinda Willard, Satya Yadav, Stefan du Plessis

Published in: Reproductive Biology and Endocrinology | Issue 1/2013

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Abstract

Background

Oxidative stress plays a key role in the etiology of male infertility. Significant alterations in the sperm proteome are associated with poor semen quality. The aim of the present study was to examine if elevated levels of reactive oxygen species cause an alteration in the proteomic profile of spermatozoa.

Methods

This prospective study consisted of 52 subjects: 32 infertile men and 20 normal donors. Seminal ejaculates were classified as ROS+ or ROS- and evaluated for their proteomic profile. Samples were pooled and subjected to LC-MS/MS analysis through in-solution digestion of proteins for peptide characterization. The expression profile of proteins present in human spermatozoa was examined using proteomic and bioinformatic analysis to elucidate the regulatory pathways of oxidative stress.

Results

Of the 74 proteins identified, 10 proteins with a 2-fold difference were overexpressed and 5 were underexpressed in the ROS+ group; energy metabolism and regulation, carbohydrate metabolic processes such as gluconeogenesis and glycolysis, protein modifications and oxidative stress regulation were some of the metabolic processes affected in ROS+ group.

Conclusions

We have identified proteins involved in a variety of functions associated with response and management of oxidative stress. In the present study we focused on proteins that showed a high degree of differential expression and thus, have a greater impact on the fertilizing potential of the spermatozoa. While proteomic analyses identified the potential biomarkers, further studies through Western Blot are necessary to validate the biomarker status of the proteins in pathological conditions.
Appendix
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Literature
1.
go back to reference Sharma R, Aaron T, Kothari S, Agarwal A: A comprehensive overview - Oxidative stress in male reproduction. Free Radical Biomedicine. Edited by: Pantopoulos K, Schipper H. 2012, Hauppauge NY: Nova Science Publishers Inc, 305-328. Chapter 13 Sharma R, Aaron T, Kothari S, Agarwal A: A comprehensive overview - Oxidative stress in male reproduction. Free Radical Biomedicine. Edited by: Pantopoulos K, Schipper H. 2012, Hauppauge NY: Nova Science Publishers Inc, 305-328. Chapter 13
2.
go back to reference Agarwal A, Cocuzza M, Abdelrazik H, Sharma RK: Oxidative stress measurement in patients with male or female factor infertility. Handbook of Chemiluminescenct Methods in Oxidative Stress Assessment. Edited by: Popov I, Lewin G. 2009, Kerala, India: Transworld Research Network, 195-218. Agarwal A, Cocuzza M, Abdelrazik H, Sharma RK: Oxidative stress measurement in patients with male or female factor infertility. Handbook of Chemiluminescenct Methods in Oxidative Stress Assessment. Edited by: Popov I, Lewin G. 2009, Kerala, India: Transworld Research Network, 195-218.
3.
go back to reference Mahfouz R, Sharma R, Thiyagarajan A, Kale V, Gupta S, Sabanegh E, Agarwal A: Semen characteristics and sperm DNA fragmentation in infertile men with low and high levels of seminal reactive oxygen species. Fertil Steril. 2003, 94: 2141-2146.CrossRef Mahfouz R, Sharma R, Thiyagarajan A, Kale V, Gupta S, Sabanegh E, Agarwal A: Semen characteristics and sperm DNA fragmentation in infertile men with low and high levels of seminal reactive oxygen species. Fertil Steril. 2003, 94: 2141-2146.CrossRef
4.
go back to reference Pasqualotto FF, Sharma RK, Nelson DR, Thomas AJ, Agarwal A: Relationship between oxidative stress, semen characteristics, and clinical diagnosis in men undergoing fertility investigation. Fertil Steril. 2000, 73: 459-464. 10.1016/S0015-0282(99)00567-1.CrossRefPubMed Pasqualotto FF, Sharma RK, Nelson DR, Thomas AJ, Agarwal A: Relationship between oxidative stress, semen characteristics, and clinical diagnosis in men undergoing fertility investigation. Fertil Steril. 2000, 73: 459-464. 10.1016/S0015-0282(99)00567-1.CrossRefPubMed
5.
go back to reference Agarwal A, Makker K, Sharma R: Clinical relevance of oxidative stress in male factor infertility: an update. Am J Reprod Immunol. 2008, 59: 2-11.CrossRefPubMed Agarwal A, Makker K, Sharma R: Clinical relevance of oxidative stress in male factor infertility: an update. Am J Reprod Immunol. 2008, 59: 2-11.CrossRefPubMed
6.
go back to reference Agarwal A, Sharma RK, Nallella KP, Thomas AJ, Alvarez JG, Sikka SC: Reactive oxygen species as an independent marker of male factor infertility. Fertil Steril. 2006, 86: 878-885. 10.1016/j.fertnstert.2006.02.111.CrossRefPubMed Agarwal A, Sharma RK, Nallella KP, Thomas AJ, Alvarez JG, Sikka SC: Reactive oxygen species as an independent marker of male factor infertility. Fertil Steril. 2006, 86: 878-885. 10.1016/j.fertnstert.2006.02.111.CrossRefPubMed
7.
go back to reference Sharma RK, Pasqualotto FF, Nelson DR, Thomas AJ, Agarwal A: The reactive oxygen species-total antioxidant capacity score is a new measure of oxidative stress to predict male infertility. Hum Reprod. 1999, 14: 2801-2807. 10.1093/humrep/14.11.2801.CrossRefPubMed Sharma RK, Pasqualotto FF, Nelson DR, Thomas AJ, Agarwal A: The reactive oxygen species-total antioxidant capacity score is a new measure of oxidative stress to predict male infertility. Hum Reprod. 1999, 14: 2801-2807. 10.1093/humrep/14.11.2801.CrossRefPubMed
8.
go back to reference Pasqualotto FF, Sharma RK, Potts JM, Nelson DR, Thomas AJ, Agarwal A: Seminal oxidative stress in patients with chronic prostatitis. Urology. 2000, 55: 881-885. 10.1016/S0090-4295(99)00613-5.CrossRefPubMed Pasqualotto FF, Sharma RK, Potts JM, Nelson DR, Thomas AJ, Agarwal A: Seminal oxidative stress in patients with chronic prostatitis. Urology. 2000, 55: 881-885. 10.1016/S0090-4295(99)00613-5.CrossRefPubMed
9.
go back to reference Agarwal A, Prabakaran S, Allamaneni SS: Relationship between oxidative stress, varicocele and infertility: a meta-analysis. Reprod Biomed Online. 2006, 12: 630-633. 10.1016/S1472-6483(10)61190-X.CrossRefPubMed Agarwal A, Prabakaran S, Allamaneni SS: Relationship between oxidative stress, varicocele and infertility: a meta-analysis. Reprod Biomed Online. 2006, 12: 630-633. 10.1016/S1472-6483(10)61190-X.CrossRefPubMed
10.
go back to reference Agarwal A, Sharma RK, Desai NR, Prabakaran S, Tavares A, Sabanegh E: Role of oxidative stress in pathogenesis of varicocele and infertility. Urology. 2009, 73: 461-469. 10.1016/j.urology.2008.07.053.CrossRefPubMed Agarwal A, Sharma RK, Desai NR, Prabakaran S, Tavares A, Sabanegh E: Role of oxidative stress in pathogenesis of varicocele and infertility. Urology. 2009, 73: 461-469. 10.1016/j.urology.2008.07.053.CrossRefPubMed
11.
go back to reference Pasqualotto FF, Sundaram A, Sharma RK, Borges E, Pasqualotto EB, Agarwal A: Semen quality and oxidative stress scores in fertile and infertile patients with varicocele. Fertil Steril. 2008, 89: 602-607. 10.1016/j.fertnstert.2007.03.057.CrossRefPubMed Pasqualotto FF, Sundaram A, Sharma RK, Borges E, Pasqualotto EB, Agarwal A: Semen quality and oxidative stress scores in fertile and infertile patients with varicocele. Fertil Steril. 2008, 89: 602-607. 10.1016/j.fertnstert.2007.03.057.CrossRefPubMed
12.
go back to reference Hamada A, Sharma R, du Plessis S, Willard B, Yadav S, Sabanegh E, Agarwal A: Two dimensional differential in-gel electrophoresis-based proteomics of male gametes in relation to oxidative stress. Fertil Steril. 2013, 99: 1216-1226. 10.1016/j.fertnstert.2012.11.046.CrossRefPubMed Hamada A, Sharma R, du Plessis S, Willard B, Yadav S, Sabanegh E, Agarwal A: Two dimensional differential in-gel electrophoresis-based proteomics of male gametes in relation to oxidative stress. Fertil Steril. 2013, 99: 1216-1226. 10.1016/j.fertnstert.2012.11.046.CrossRefPubMed
13.
go back to reference Vazquez L, Mónica H: Proteomic analysis and sperm physiopathology: the two-dimensional difference in gel electrophoresis approach. Fertil Steril. 2013, 99: 1199-1200. 10.1016/j.fertnstert.2012.12.051.CrossRef Vazquez L, Mónica H: Proteomic analysis and sperm physiopathology: the two-dimensional difference in gel electrophoresis approach. Fertil Steril. 2013, 99: 1199-1200. 10.1016/j.fertnstert.2012.12.051.CrossRef
14.
go back to reference de Mateo S, Estanyol JM, Oliva R: Methods for the analysis of the sperm proteome. Methods Mol Biol. 2013, 927: 411-422. 10.1007/978-1-62703-038-0_35.CrossRefPubMed de Mateo S, Estanyol JM, Oliva R: Methods for the analysis of the sperm proteome. Methods Mol Biol. 2013, 927: 411-422. 10.1007/978-1-62703-038-0_35.CrossRefPubMed
15.
go back to reference de Mateo S, Martínez-Heredia J, Estanyol JM, Domínguez-Fandos D, Vidal-Taboada JM, Ballescà JL, Oliva R: Marked correlations in protein expression identified by proteomic analysis of human spermatozoa. Proteomics. 2007, 7: 4264-4277. 10.1002/pmic.200700521.CrossRefPubMed de Mateo S, Martínez-Heredia J, Estanyol JM, Domínguez-Fandos D, Vidal-Taboada JM, Ballescà JL, Oliva R: Marked correlations in protein expression identified by proteomic analysis of human spermatozoa. Proteomics. 2007, 7: 4264-4277. 10.1002/pmic.200700521.CrossRefPubMed
16.
go back to reference Oliva R, De Mateo S, Castillo J, Azpiazu R, Oriola J, Ballescà JL: Methodological advances in sperm proteomics. Hum Fertil. 2010, 13: 263-267. 10.3109/14647273.2010.516877.CrossRef Oliva R, De Mateo S, Castillo J, Azpiazu R, Oriola J, Ballescà JL: Methodological advances in sperm proteomics. Hum Fertil. 2010, 13: 263-267. 10.3109/14647273.2010.516877.CrossRef
18.
go back to reference Govindaraju A, Dogan S, Rodriguez-Osorio N, Grant K, Kaya A, Memili E: Delivering value from sperm proteomics for fertility. Cell Tissue Res. 2012, 349: 783-793. 10.1007/s00441-012-1452-2.CrossRefPubMed Govindaraju A, Dogan S, Rodriguez-Osorio N, Grant K, Kaya A, Memili E: Delivering value from sperm proteomics for fertility. Cell Tissue Res. 2012, 349: 783-793. 10.1007/s00441-012-1452-2.CrossRefPubMed
19.
go back to reference Baker MA, Nixon B, Naumovski N, Aitken RJ: Proteomic insights into the maturation and capacitation of mammalian spermatozoa. Syst Biol Reprod Med. 2012, 58: 211-217. 10.3109/19396368.2011.639844.CrossRefPubMed Baker MA, Nixon B, Naumovski N, Aitken RJ: Proteomic insights into the maturation and capacitation of mammalian spermatozoa. Syst Biol Reprod Med. 2012, 58: 211-217. 10.3109/19396368.2011.639844.CrossRefPubMed
20.
go back to reference Parte PP, Rao P, Redij S, Lobo V, D’Souza SJ, Gajbhiye R, Kulkarni V: Sperm phosphoproteome profiling by ultra performance liquid chromatography followed by data independent analysis (LC-MS(E)) reveals altered proteomic signatures in asthenozoospermia. J Proteomics. 2012, 75: 5861-5871. 10.1016/j.jprot.2012.07.003.CrossRefPubMed Parte PP, Rao P, Redij S, Lobo V, D’Souza SJ, Gajbhiye R, Kulkarni V: Sperm phosphoproteome profiling by ultra performance liquid chromatography followed by data independent analysis (LC-MS(E)) reveals altered proteomic signatures in asthenozoospermia. J Proteomics. 2012, 75: 5861-5871. 10.1016/j.jprot.2012.07.003.CrossRefPubMed
21.
go back to reference Baker MA, Naumovski N, Hetherington L, Weinberg A, Velkov T, Aitken RJ: Head and flagella subcompartmental proteomic analysis of human spermatozoa. Proteomics. 2013, 13: 61-74. 10.1002/pmic.201200350.CrossRefPubMed Baker MA, Naumovski N, Hetherington L, Weinberg A, Velkov T, Aitken RJ: Head and flagella subcompartmental proteomic analysis of human spermatozoa. Proteomics. 2013, 13: 61-74. 10.1002/pmic.201200350.CrossRefPubMed
22.
go back to reference World Health Organization: WHO Laboratory Manual for the Examination and Processing of Human Semen. 5th ed. 2010, Cambridge: World Health Organization, 5 World Health Organization: WHO Laboratory Manual for the Examination and Processing of Human Semen. 5th ed. 2010, Cambridge: World Health Organization, 5
23.
go back to reference Benjamin D, Sharma RK, Moazzam A, Agarwal A: Methods for the detection of ROS in human sperm samples. Studies on Men’s Health and Fertility. Edited by: Agarwal A, Aitken RJ, Alvarez JG. 2012, New York, NY: Springer Science+Business Media, 257-273.CrossRef Benjamin D, Sharma RK, Moazzam A, Agarwal A: Methods for the detection of ROS in human sperm samples. Studies on Men’s Health and Fertility. Edited by: Agarwal A, Aitken RJ, Alvarez JG. 2012, New York, NY: Springer Science+Business Media, 257-273.CrossRef
24.
go back to reference Boyle E, Weng S, Gollub J, Jin H, Botstein D, Cherry JM, Sherlock G: GO: TermFinder-open source software for accessing Gene Ontology information and finding significantly enriched Gene Ontology terms associated with a list of genes. Bioinformatics. 2004, 20: 3710-3715. 10.1093/bioinformatics/bth456.PubMedCentralCrossRefPubMed Boyle E, Weng S, Gollub J, Jin H, Botstein D, Cherry JM, Sherlock G: GO: TermFinder-open source software for accessing Gene Ontology information and finding significantly enriched Gene Ontology terms associated with a list of genes. Bioinformatics. 2004, 20: 3710-3715. 10.1093/bioinformatics/bth456.PubMedCentralCrossRefPubMed
26.
go back to reference The UniProt Consortium: Reorganizing the protein space at the Universal Protein Resource (UniProt). Nucleic Acids Res. 2011, 40: D71-D75.PubMedCentralCrossRef The UniProt Consortium: Reorganizing the protein space at the Universal Protein Resource (UniProt). Nucleic Acids Res. 2011, 40: D71-D75.PubMedCentralCrossRef
27.
go back to reference Bhatia VN, Perlman DH, Costello CE, McComb ME: Software tool for researching annotations of proteins: open-source protein annotation software with data visualization. Anal Chem. 2009, 81: 9819-9823. 10.1021/ac901335x.PubMedCentralCrossRefPubMed Bhatia VN, Perlman DH, Costello CE, McComb ME: Software tool for researching annotations of proteins: open-source protein annotation software with data visualization. Anal Chem. 2009, 81: 9819-9823. 10.1021/ac901335x.PubMedCentralCrossRefPubMed
28.
go back to reference Wu C, Orozco C, Boyer J, Leglise M, Goodale J, Batalov S, Hodge CL, Haase J, Janes J, Huss JW, Su AI: BioGPS: an extensible and customizable portal for querying and organizing gene annotation resources. Genome Biol. 2009, 10: R130-10.1186/gb-2009-10-11-r130.PubMedCentralCrossRefPubMed Wu C, Orozco C, Boyer J, Leglise M, Goodale J, Batalov S, Hodge CL, Haase J, Janes J, Huss JW, Su AI: BioGPS: an extensible and customizable portal for querying and organizing gene annotation resources. Genome Biol. 2009, 10: R130-10.1186/gb-2009-10-11-r130.PubMedCentralCrossRefPubMed
31.
go back to reference Martínez-Heredia J, de Mateo S, Vidal-Taboada JM, Ballescà JL, Oliva R: Identification of proteomic differences in asthenozoospermic sperm samples. Hum Reprod. 2008, 23: 783-791. 10.1093/humrep/den024.CrossRefPubMed Martínez-Heredia J, de Mateo S, Vidal-Taboada JM, Ballescà JL, Oliva R: Identification of proteomic differences in asthenozoospermic sperm samples. Hum Reprod. 2008, 23: 783-791. 10.1093/humrep/den024.CrossRefPubMed
32.
go back to reference de Yebra L, Ballescá JL, Vanrell JA, Corzett M, Balhorn R, Oliva R: Detection of P2 precursors in the sperm cells of infertile patients who have reduced protamine P2 levels. Fertil Steril. 1998, 69: 755-759. 10.1016/S0015-0282(98)00012-0.CrossRefPubMed de Yebra L, Ballescá JL, Vanrell JA, Corzett M, Balhorn R, Oliva R: Detection of P2 precursors in the sperm cells of infertile patients who have reduced protamine P2 levels. Fertil Steril. 1998, 69: 755-759. 10.1016/S0015-0282(98)00012-0.CrossRefPubMed
33.
go back to reference Zhao C, Huo R, Wang FQ, Lin M, Zhou ZM, Sha JH: Identification of several proteins involved in regulation of sperm motility by proteomic analysis. Fertil Steril. 2007, 87: 436-438. 10.1016/j.fertnstert.2006.06.057.CrossRefPubMed Zhao C, Huo R, Wang FQ, Lin M, Zhou ZM, Sha JH: Identification of several proteins involved in regulation of sperm motility by proteomic analysis. Fertil Steril. 2007, 87: 436-438. 10.1016/j.fertnstert.2006.06.057.CrossRefPubMed
34.
go back to reference Rajeev SK, Reddy KV: Sperm membrane protein profiles of fertile and infertile men: identification and characterization of fertility-associated sperm antigen. Hum Reprod. 2004, 19: 234-242. 10.1093/humrep/deh066.CrossRefPubMed Rajeev SK, Reddy KV: Sperm membrane protein profiles of fertile and infertile men: identification and characterization of fertility-associated sperm antigen. Hum Reprod. 2004, 19: 234-242. 10.1093/humrep/deh066.CrossRefPubMed
35.
go back to reference Xu W, Hu H, Wang Z, Chen X, Yang F, Zhu Z, Fang P, Dai J, Wang L, Shi H, Li Z, Qiao Z: Proteomic characteristics of spermatozoa in normozoospermic patients with infertility. J Proteomics. 2012, 75: 5426-5436. 10.1016/j.jprot.2012.06.021.CrossRefPubMed Xu W, Hu H, Wang Z, Chen X, Yang F, Zhu Z, Fang P, Dai J, Wang L, Shi H, Li Z, Qiao Z: Proteomic characteristics of spermatozoa in normozoospermic patients with infertility. J Proteomics. 2012, 75: 5426-5436. 10.1016/j.jprot.2012.06.021.CrossRefPubMed
36.
go back to reference Nakamura N, Mori C, Eddy EM: Molecular complex of three testis-specific isozymes associated with the mouse sperm fibrous sheath: hexokinase 1, phosphofructokinase M, and glutathione S-transferase mu class 5. Biol Reprod. 2010, 82: 504-515. 10.1095/biolreprod.109.080580.PubMedCentralCrossRefPubMed Nakamura N, Mori C, Eddy EM: Molecular complex of three testis-specific isozymes associated with the mouse sperm fibrous sheath: hexokinase 1, phosphofructokinase M, and glutathione S-transferase mu class 5. Biol Reprod. 2010, 82: 504-515. 10.1095/biolreprod.109.080580.PubMedCentralCrossRefPubMed
37.
go back to reference Nascimento JM, Shi LZ, Tam J, Chandsawangbhuwana C, Durrant B, Botvinick EL, Berns MW: Comparison of glycolysis and oxidative phosphorylation as energy sources for mammalian sperm motility, using the combination of fluorescence imaging, laser tweezers, and real-time automated tracking and trapping. J Cell Physiol. 2008, 217: 745-751. 10.1002/jcp.21549.PubMedCentralCrossRefPubMed Nascimento JM, Shi LZ, Tam J, Chandsawangbhuwana C, Durrant B, Botvinick EL, Berns MW: Comparison of glycolysis and oxidative phosphorylation as energy sources for mammalian sperm motility, using the combination of fluorescence imaging, laser tweezers, and real-time automated tracking and trapping. J Cell Physiol. 2008, 217: 745-751. 10.1002/jcp.21549.PubMedCentralCrossRefPubMed
38.
go back to reference Storey BT: Mammalian sperm metabolism: oxygen and sugar, friend and foe. Int J Dev Biol. 2008, 52: 427-437. 10.1387/ijdb.072522bs.CrossRefPubMed Storey BT: Mammalian sperm metabolism: oxygen and sugar, friend and foe. Int J Dev Biol. 2008, 52: 427-437. 10.1387/ijdb.072522bs.CrossRefPubMed
39.
go back to reference Terrell KA, Wildt DE, Anthony NM, Bavister BD, Leibo SP, Penfold LM, Marker LL, Crosier AE: Oxidative phosphorylation is essential for felid sperm function, but is substantially lower in cheetah (Acinonyx jubatus) compared to domestic cat (Felis catus) ejaculate. Biol Reprod. 2011, 85: 473-481. 10.1095/biolreprod.111.092106.CrossRefPubMed Terrell KA, Wildt DE, Anthony NM, Bavister BD, Leibo SP, Penfold LM, Marker LL, Crosier AE: Oxidative phosphorylation is essential for felid sperm function, but is substantially lower in cheetah (Acinonyx jubatus) compared to domestic cat (Felis catus) ejaculate. Biol Reprod. 2011, 85: 473-481. 10.1095/biolreprod.111.092106.CrossRefPubMed
40.
go back to reference Elkina YL, Atroshchenko MM, Bragina EE, Muronetz VI, Schmalhausen EV: Oxidation of glyceraldehyde-3-phosphate dehydrogenase decreases sperm motility. Biochemistry. 2011, 76: 268-272.PubMed Elkina YL, Atroshchenko MM, Bragina EE, Muronetz VI, Schmalhausen EV: Oxidation of glyceraldehyde-3-phosphate dehydrogenase decreases sperm motility. Biochemistry. 2011, 76: 268-272.PubMed
41.
go back to reference Sharma R, Agarwal A: Spermatogenesis: An overview. Human sperm chromatin: Structure and Function. Sperm Chromatin. Biological and Clinical Applications in Male Infertility and Assisted Reproduction. Edited by: Zini A, Agarwal A. 2012, New York: Springer Science + Business Media, 19-44. Sharma R, Agarwal A: Spermatogenesis: An overview. Human sperm chromatin: Structure and Function. Sperm Chromatin. Biological and Clinical Applications in Male Infertility and Assisted Reproduction. Edited by: Zini A, Agarwal A. 2012, New York: Springer Science + Business Media, 19-44.
42.
go back to reference Lilja H, Abrahamsson PA, Lundwall A: Semenogelin, the predominant protein in human semen. Primary structure and identification of closely related proteins in the male accessory sex glands and on the spermatozoa. J Biol Chem. 1989, 264: 1894-1900.PubMed Lilja H, Abrahamsson PA, Lundwall A: Semenogelin, the predominant protein in human semen. Primary structure and identification of closely related proteins in the male accessory sex glands and on the spermatozoa. J Biol Chem. 1989, 264: 1894-1900.PubMed
43.
go back to reference Lilja H, Lundwall A: Molecular cloning of epididymal and seminal vesicular transcripts encoding a semenogelin-related protein. Proc Natl Acad Sci USA. 1992, 89: 4559-4563. 10.1073/pnas.89.10.4559.PubMedCentralCrossRefPubMed Lilja H, Lundwall A: Molecular cloning of epididymal and seminal vesicular transcripts encoding a semenogelin-related protein. Proc Natl Acad Sci USA. 1992, 89: 4559-4563. 10.1073/pnas.89.10.4559.PubMedCentralCrossRefPubMed
44.
go back to reference de Lamirande E, Yoshida K, Yoshiike TM, Iwamoto T, Gagnon C: Semenogelin, the main protein of semen coagulum, inhibits human sperm capacitation by interfering with the superoxide anion generated during this process. J Androl. 2001, 22: 672-679.PubMed de Lamirande E, Yoshida K, Yoshiike TM, Iwamoto T, Gagnon C: Semenogelin, the main protein of semen coagulum, inhibits human sperm capacitation by interfering with the superoxide anion generated during this process. J Androl. 2001, 22: 672-679.PubMed
45.
go back to reference Auger J, Eustache F, Maceiras P, Broussard C, Chafey P, Lesaffre C, Vaiman D, Camoin L, Auer J: Modified expression of several sperm proteins after chronic exposure to the antiandrogenic compound vinclozolin. Toxicol Sci. 2010, 117: 475-484. 10.1093/toxsci/kfq199.CrossRefPubMed Auger J, Eustache F, Maceiras P, Broussard C, Chafey P, Lesaffre C, Vaiman D, Camoin L, Auer J: Modified expression of several sperm proteins after chronic exposure to the antiandrogenic compound vinclozolin. Toxicol Sci. 2010, 117: 475-484. 10.1093/toxsci/kfq199.CrossRefPubMed
46.
go back to reference Feder ME, Hofmann GE: Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu Rev Physiol. 1999, 61: 243-282. 10.1146/annurev.physiol.61.1.243.CrossRefPubMed Feder ME, Hofmann GE: Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu Rev Physiol. 1999, 61: 243-282. 10.1146/annurev.physiol.61.1.243.CrossRefPubMed
47.
go back to reference Katschinski DM: On heat and cells and proteins. News Physiol Sci. 2004, 19: 11-15.PubMed Katschinski DM: On heat and cells and proteins. News Physiol Sci. 2004, 19: 11-15.PubMed
48.
go back to reference Sung DY, Guy CL: Physiological and molecular assessment of altered expression of Hsc70-1 in Arabidopsis. Evidence for pleiotropic consequences. Plant Physiol. 2003, 132: 979-987. 10.1104/pp.102.019398.PubMedCentralCrossRefPubMed Sung DY, Guy CL: Physiological and molecular assessment of altered expression of Hsc70-1 in Arabidopsis. Evidence for pleiotropic consequences. Plant Physiol. 2003, 132: 979-987. 10.1104/pp.102.019398.PubMedCentralCrossRefPubMed
49.
go back to reference Folk JE: Transglutaminases. Annu Rev Biochem. 1980, 49: 517-531. 10.1146/annurev.bi.49.070180.002505.CrossRefPubMed Folk JE: Transglutaminases. Annu Rev Biochem. 1980, 49: 517-531. 10.1146/annurev.bi.49.070180.002505.CrossRefPubMed
50.
51.
go back to reference Shin DM, Jeon JH, Kim CW, Cho SY, Lee HJ, Jang GY, Jeong EM, Lee DS, Kang JH, Melino G, Park SC, Kim IG: TGF beta mediates activation of transglutaminase 2 in response to oxidative stress that leads to protein aggregation. FASEB J. 2008, 22: 2498-2507. 10.1096/fj.07-095455.CrossRefPubMed Shin DM, Jeon JH, Kim CW, Cho SY, Lee HJ, Jang GY, Jeong EM, Lee DS, Kang JH, Melino G, Park SC, Kim IG: TGF beta mediates activation of transglutaminase 2 in response to oxidative stress that leads to protein aggregation. FASEB J. 2008, 22: 2498-2507. 10.1096/fj.07-095455.CrossRefPubMed
52.
go back to reference Li Y, Okumura K, Nomura S, Maeda N, Miyasho T, Yokota H: Oxidatively damaged proteins in the early stage of testicular toxicities in male rats by orally administered with a synthetic oestrogen, diethylstilbestrol. Reprod Toxicol. 2011, 31: 26-34. 10.1016/j.reprotox.2010.09.007.CrossRefPubMed Li Y, Okumura K, Nomura S, Maeda N, Miyasho T, Yokota H: Oxidatively damaged proteins in the early stage of testicular toxicities in male rats by orally administered with a synthetic oestrogen, diethylstilbestrol. Reprod Toxicol. 2011, 31: 26-34. 10.1016/j.reprotox.2010.09.007.CrossRefPubMed
53.
go back to reference Immenschuh S, Baumgart-Vogt E, Tan M, Iwahara S, Ramadori G, Fahimi HD: Differential cellular and subcellular localization of heme-binding protein 23/peroxiredoxin I and heme oxygenase-1 in rat liver. J Histochem Cytochem. 2003, 51: 1621-1631. 10.1177/002215540305101206.CrossRefPubMed Immenschuh S, Baumgart-Vogt E, Tan M, Iwahara S, Ramadori G, Fahimi HD: Differential cellular and subcellular localization of heme-binding protein 23/peroxiredoxin I and heme oxygenase-1 in rat liver. J Histochem Cytochem. 2003, 51: 1621-1631. 10.1177/002215540305101206.CrossRefPubMed
54.
go back to reference Wood ZA, Poole LB, Karplus PA: Peroxiredoxin evolution and the regulation of hydrogen peroxide signaling. Science. 2003, 300: 650-653. 10.1126/science.1080405.CrossRefPubMed Wood ZA, Poole LB, Karplus PA: Peroxiredoxin evolution and the regulation of hydrogen peroxide signaling. Science. 2003, 300: 650-653. 10.1126/science.1080405.CrossRefPubMed
55.
go back to reference O’Flaherty C, de Souza AR: Hydrogen peroxide modifies human sperm peroxiredoxins in a dose-dependent manner. Biol Reprod. 2011, 84: 238-247. 10.1095/biolreprod.110.085712.PubMedCentralCrossRefPubMed O’Flaherty C, de Souza AR: Hydrogen peroxide modifies human sperm peroxiredoxins in a dose-dependent manner. Biol Reprod. 2011, 84: 238-247. 10.1095/biolreprod.110.085712.PubMedCentralCrossRefPubMed
56.
go back to reference Gong S, Gabriel MC, Zini A, Chan P, O’Flaherty C: Low amounts and high thiol oxidation of peroxiredoxins in spermatozoa from infertile men. J Androl. 2012, 33: 1342-1351. 10.2164/jandrol.111.016162.CrossRefPubMed Gong S, Gabriel MC, Zini A, Chan P, O’Flaherty C: Low amounts and high thiol oxidation of peroxiredoxins in spermatozoa from infertile men. J Androl. 2012, 33: 1342-1351. 10.2164/jandrol.111.016162.CrossRefPubMed
57.
go back to reference Rey RA, Musse M, Venara M, Chemes HE: Ontogeny of the androgen receptor expression in the fetal and postnatal testis: its relevance on Sertoli cell maturation and the onset of adult spermatogenesis. Microsc Res Tech. 2009, 72: 787-795. 10.1002/jemt.20754.CrossRefPubMed Rey RA, Musse M, Venara M, Chemes HE: Ontogeny of the androgen receptor expression in the fetal and postnatal testis: its relevance on Sertoli cell maturation and the onset of adult spermatogenesis. Microsc Res Tech. 2009, 72: 787-795. 10.1002/jemt.20754.CrossRefPubMed
58.
go back to reference Stanton PG, Sluka P, Foo CF, Stephens AN, Smith AI, McLachlan RI, O’Donnell L: Proteomic changes in rat spermatogenesis in response to in vivo androgen manipulation; impact on meiotic cells. PLoS One. 2012, 7: e41718-10.1371/journal.pone.0041718.PubMedCentralCrossRefPubMed Stanton PG, Sluka P, Foo CF, Stephens AN, Smith AI, McLachlan RI, O’Donnell L: Proteomic changes in rat spermatogenesis in response to in vivo androgen manipulation; impact on meiotic cells. PLoS One. 2012, 7: e41718-10.1371/journal.pone.0041718.PubMedCentralCrossRefPubMed
59.
go back to reference Wang RS, Yeh S, Tzeng CR, Chang C: Androgen receptor roles in spermatogenesis and fertility: lessons from testicular cell-specific androgen receptor knockout mice. Endocr Rev. 2009, 30: 119-132. 10.1210/er.2008-0025.PubMedCentralCrossRefPubMed Wang RS, Yeh S, Tzeng CR, Chang C: Androgen receptor roles in spermatogenesis and fertility: lessons from testicular cell-specific androgen receptor knockout mice. Endocr Rev. 2009, 30: 119-132. 10.1210/er.2008-0025.PubMedCentralCrossRefPubMed
60.
go back to reference Singh J, O’Neill C, Handelsman DJ: Induction of spermatogenesis by androgens in gonadotropin-deficient (hpg) mice. Endocrinology. 1995, 136: 5311-5321. 10.1210/en.136.12.5311.PubMed Singh J, O’Neill C, Handelsman DJ: Induction of spermatogenesis by androgens in gonadotropin-deficient (hpg) mice. Endocrinology. 1995, 136: 5311-5321. 10.1210/en.136.12.5311.PubMed
61.
go back to reference Tamai KT, Monaco L, Nantel F, Zazopoulos E, Sassone-Corsi P: Coupling signalling pathways to transcriptional control: nuclear factors responsive to cAMP. Recent Prog Horm Res. 1997, 52: 121-139. discussion 139-40PubMed Tamai KT, Monaco L, Nantel F, Zazopoulos E, Sassone-Corsi P: Coupling signalling pathways to transcriptional control: nuclear factors responsive to cAMP. Recent Prog Horm Res. 1997, 52: 121-139. discussion 139-40PubMed
62.
go back to reference Hogeveen KN, Sassone-Corsi P: Regulation of gene expression in post-meiotic male germ cells: CREM-signalling pathways and male fertility. Hum Fertil. 2006, 9: 73-79. 10.1080/14647270500463400.CrossRef Hogeveen KN, Sassone-Corsi P: Regulation of gene expression in post-meiotic male germ cells: CREM-signalling pathways and male fertility. Hum Fertil. 2006, 9: 73-79. 10.1080/14647270500463400.CrossRef
63.
go back to reference Monaco L, Kotaja N, Fienga G, Hogeveen K, Kolthur US, Kimmins S, Brancorsini S, Macho B, Sassone-Corsi P: Specialized rules of gene transcription in male germ cells: the CREM paradigm. Int J Androl. 2004, 27: 322-327. 10.1111/j.1365-2605.2004.00494.x.CrossRefPubMed Monaco L, Kotaja N, Fienga G, Hogeveen K, Kolthur US, Kimmins S, Brancorsini S, Macho B, Sassone-Corsi P: Specialized rules of gene transcription in male germ cells: the CREM paradigm. Int J Androl. 2004, 27: 322-327. 10.1111/j.1365-2605.2004.00494.x.CrossRefPubMed
64.
go back to reference Weinbauer GF, Behr R, Bergmann M, Nieschlag E: Testicular cAMP responsive element modulator (CREM) protein is expressed in round spermatids but is absent or reduced in men with round spermatid maturation arrest. Mol Hum Reprod. 1998, 4: 9-15. 10.1093/molehr/4.1.9.CrossRefPubMed Weinbauer GF, Behr R, Bergmann M, Nieschlag E: Testicular cAMP responsive element modulator (CREM) protein is expressed in round spermatids but is absent or reduced in men with round spermatid maturation arrest. Mol Hum Reprod. 1998, 4: 9-15. 10.1093/molehr/4.1.9.CrossRefPubMed
Metadata
Title
Proteomic analysis of human spermatozoa proteins with oxidative stress
Authors
Rakesh Sharma
Ashok Agarwal
Gayatri Mohanty
Alaa J Hamada
Banu Gopalan
Belinda Willard
Satya Yadav
Stefan du Plessis
Publication date
01-12-2013
Publisher
BioMed Central
Published in
Reproductive Biology and Endocrinology / Issue 1/2013
Electronic ISSN: 1477-7827
DOI
https://doi.org/10.1186/1477-7827-11-48

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