Testicular phosphoproteome in perfluorododecanoic acid-exposed rats

Toxicology Letters

Volumn 221, Issue 2, 2013, Pages 91-101

  Shi, Zhimin ^a   Hou, Junjie ^b   Guo, Xuejiang ^c   Zhang, Hongxia ^a   Yang, Fuquan ^b   Dai, Jiayin ^a  

^a INSTITUTE OF ZOOLOGY   (China)

^b INSTITUTE OF BIOPHYSICS   (China)

^c NANJING MEDICAL UNIVERSITY   (China)

Author keywords

CDC2; MAPK; PFDoA; Phosphoproteome; Testes

Indexed keywords

CELL CYCLE PROTEIN; CELL CYCLE PROTEIN 2; MITOGEN ACTIVATED PROTEIN KINASE; PERFLUORODECANOIC ACID; PERFLUORODODECANOIC ACID; PHOSPHOPEPTIDE; PHOSPHOPROTEOME; TITANIUM DIOXIDE; UNCLASSIFIED DRUG; CDK1 PROTEIN, RAT; CYCLIN DEPENDENT KINASE; LAURIC ACID DERIVATIVE; PROTEOME;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; FRACTIONATION; IMMOBILIZED METAL AFFINITY CHROMATOGRAPHY; IN VITRO STUDY; LEYDIG CELL; LIQUID CHROMATOGRAPHY; MALE; NONHUMAN; POLLUTANT; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN PHOSPHORYLATION; RAT; SPERM; SPERMATOGENESIS; TANDEM MASS SPECTROMETRY; TESTIS FUNCTION; ANIMAL; BIOLOGY; DRUG EFFECTS; GENETICS; METABOLISM; PHOSPHORYLATION; SPRAGUE DAWLEY RAT; TOXICITY;

ANIMALS; CHROMATOGRAPHY, LIQUID; COMPUTATIONAL BIOLOGY; CYCLIN-DEPENDENT KINASES; LAURIC ACIDS; LEYDIG CELLS; MALE; MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHOPEPTIDES; PHOSPHORYLATION; PROTEOME; RATS; RATS, SPRAGUE-DAWLEY; SPERMATOGENESIS; TANDEM MASS SPECTROMETRY;

EID: 84880381166     PISSN: 03784274     EISSN: 18793169     Source Type: Journal    
DOI: 10.1016/j.toxlet.2013.06.219     Document Type: Article

References (45)

1. Adinolfi E., Callegari M.G., Ferrari D., Bolognesi C., Minelli M., Wieckowski M.R., et al. Basal activation of the P2X7 ATP receptor elevates mitochondrial calcium and potential, increases cellular ATP levels, and promotes serum-independent growth. Molecular Biology of the Cell 2005, 16:3260-3272.
2. Alekseev O.M., Richardson R.T., O'Rand M.G. Linker histones stimulate HSPA2 ATPase activity through NASP binding and inhibit CDC2/Cyclin B1 complex formation during meiosis in the mouse. Biology of Reproduction 2009, 81:739-748.
3. Almog T., Naor Z. The role of mitogen activated protein kinase (MAPK) in sperm functions. Molecular and Cellular Endocrinology 2010, 314:239-243.
4. Andric S.A., Janjic M.M., Stojkov N.J., Kostic T.S. Protein kinase G-mediated stimulation of basal Leydig cell steroidogenesis. American Journal of Physiology: Endocrinology and Metabolism 2007, 293:E1399-E1408.
5. Beausoleil S.A., Villen J., Gerber S.A., Rush J., Gygi S.P. A probability-based approach for high-throughput protein phosphorylation analysis and site localization. Nature Biotechnology 2006, 24:1285-1292.
6. Bijur G.N., Jope R.S. Rapid accumulation of Akt in mitochondria following phosphatidylinositol 3-kinase activation. Journal of Neurochemistry 2003, 87:1427-1435.
7. Carr D.W., Newell A.E. The role of A-kinase anchoring proteins (AKaps) in regulating sperm function. Society of Reproduction and Fertility Supplement 2007, 63:135-141.
8. Cassimeris L. Accessory protein regulation of microtubule dynamics throughout the cell cycle. Current Opinion in Cell Biology 1999, 11:134-141.
9. Chen W.S., Xu P.Z., Gottlob K., Chen M.L., Sokol K., Shiyanova T., et al. Growth retardation and increased apoptosis in mice with homozygous disruption of the Akt1 gene. Genes and Development 2001, 15:2203-2208.
10. Cui Z., Chen X., Lu B., Park S.K., Xu T., et al. Preliminary quantitative profile of differential protein expression between rat L6 myoblasts and myotubes by stable isotope labeling with amino acids in cell culture. Proteomics 2009, 9:1274-1292.
11. Devkota B., Sasaki M., Matsui M., Takahashi K., Matsuzaki S., Koseki T., et al. Effects of scrotal insulation and pathological lesions on alpha-Smooth Muscle Actin (SMA) and vimentin in the bull testes. Journal of Reproduction and Development 2010, 56:187-190.
12. Eng J.K., McCormack A., Yates J.R. An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database. Journal of the American Society for Mass Spectrometry 1994, 5:976-989.
13. Erlichman J., Gutierrez-Juarez R., Zucker S., Mei X., Orr G.A. Developmental expression of the protein kinase C substrate/binding protein (clone 72/SSeCKS) in rat testis identification as a scaffolding protein containing an A-kinase-anchoring domain which is expressed during late-stage spermatogenesis. European Journal of Biochemistry 1999, 263:797-805.
14. Evaul K., Hammes S.R. Cross-talk between G protein-coupled and epidermal growth factor receptors regulates gonadotropin-mediated steroidogenesis in Leydig cells. Journal of Biological Chemistry 2008, 283:27525-27533.
15. Ficarro S., Chertihin O., Westbrook V.A., White F., Jayes F., Kalab P., et al. Phosphoproteome analysis of capacitated human sperm. Evidence of tyrosine phosphorylation of a kinase-anchoring protein 3 and valosin-containing protein/p97 during capacitation. Journal of Biological Chemistry 2003, 278:11579-11589.
16. Guruge K.S., Taniyasu S., Yamashita N., Wijeratna S., Mohotti K.M., Seneviratne H.R., et al. Perfluorinated organic compounds in human blood serum and seminal plasma: a study of urban and rural tea worker populations in Sri Lanka. Journal of Environmental Monitoring 2005, 7:371-377.
17. Hojlund K., Bowen B.P., Hwang H., Flynn C.R., Madireddy L., Geetha T., et al. In vivo phosphoproteome of human skeletal muscle revealed by phosphopeptide enrichment and HPLC-ESI-MS/MS. Journal of Proteome Research 2009, 8:4954-4965.
18. Hou J., Cui Z., Xie Z., Xue P., Wu P., Chen X., et al. Phosphoproteome analysis of rat L6 myotubes using reversed-phase C18 prefractionation and titanium dioxide enrichment. Journal of Proteome Research 2010, 9:777-788.
19. Jha K.N., Salicioni A.M., Arcelay E., Chertihin O., Kumari S., Herr J.C., et al. Evidence for the involvement of proline-directed serine/threonine phosphorylation in sperm capacitation. Molecular Human Reproduction 2006, 12:781-789.
20. Jung J.H., Pendergast A.M., Zipfel P.A., Traugh J.A. Phosphorylation of c-Abl by protein kinase Pak2 regulates differential binding of ABI2 and CRK. Biochemistry 2008, 47:1094-1104.
21. Kennedy G.L., Butenhoff J.L., Olsen G.W., O'Connor J.C., Seacat A.M., Perkins R.G., et al. The toxicology of perfluorooctanoate. Critical Reviews in Toxicology 2004, 34:351-384.
22. Klinefelter G.R., Hall P.F., Ewing L.L. Effect of luteinizing hormone deprivation in situ on steroidogenesis of rat Leydig cells purified by a multistep procedure. Biology of Reproduction 1987, 36:769-783.
23. Li R., Tang X.L., Miao S.Y., Zong S.D., Wang L.F. Regulation of the G2/M phase of the cell cycle by sperm associated antigen 8 (SPAG8) protein. Cell Biochemistry and Function 2009, 27:264-268.
24. Linding R., Jensen L.J., Pasculescu A., Olhovsky M., Colwill K., Bork P., et al. NetworKIN: a resource for exploring cellular phosphorylation networks. Nucleic Acids Research 2008, 36:D695-D699.
25. Maere S., Heymans K., Kuiper M. BiNGO: a Cytoscape plugin to assess overrepresentation of gene ontology categories in biological networks. Bioinformatics 2005, 21:3448-3449.
26. Mariappa D., Siva A.B., Shivaji S., Seshagiri P.B. Tyrphostin-A47 inhibitable tyrosine phosphorylation of flagellar proteins is associated with distinct alteration of motility pattern in hamster spermatozoa. Molecular Reproduction and Development 2006, 73:215-225.
27. Meroni S.B., Riera M.F., Pellizzari E.H., Cigorraga S.B. Regulation of rat Sertoli cell function by FSH: possible role of phosphatidylinositol 3-kinase/protein kinase B pathway. Journal of Endocrinology 2002, 174:195-204.
28. Mondillo C., Pagotto R.M., Piotrkowski B., Reche C.G., Patrignani Z.J., Cymeryng C.B., et al. Involvement of nitric oxide synthase in the mechanism of histamine-induced inhibition of Leydig cell steroidogenesis via histamine receptor subtypes in Sprague-Dawley rats. Biology of Reproduction 2009, 80:144-152.
29. Nolan M.A., Babcock D.F., Wennemuth G., Brown W., Burton K.A., McKnight G.S. Sperm-specific protein kinase A catalytic subunit Calpha2 orchestrates cAMP signaling for male fertility. Proceedings of the National Academy of Sciences of the United States of America 2004, 101:13483-13488.
30. Olsen J.V., Blagoev B., Gnad F., Macek B., Kumar C., Mortensen P., et al. Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell 2006, 127:635-648.
31. Rose K.L., Li A., Zalenskaya I., Zhang Y., Unni E., Hodgson K.C., et al. C-terminal phosphorylation of murine testis-specific histone H1t in elongating spermatids. Journal of Proteome Research 2008, 7:4070-4078.
32. Saribek B., Jin Y., Saigo M., Eto K., Abe S. HSP90b is involved in signaling prolactin-induced apoptosis in newt testis. Biochemical and Biophysical Research Communications 2006, 349:1190-1197.
33. Schwartz D., Gygi S.P. An iterative statistical approach to the identification of protein phosphorylation motifs from large-scale data sets. Nature Biotechnology 2005, 23:1391-1398.
34. 2-treated lens epithelial cells. Molecular Vision 2005, 11:764-774.
35. Shi Z., Ding L., Zhang H., Feng Y., Xu M., Dai J. Chronic exposure to perfluorododecanoic acid disrupts testicular steroidogenesis and the expression of related genes in male rats. Toxicology Letters 2009, 188:192-200.
36. Shi Z., Feng Y., Wang J., Zhang H., Ding L., Dai J. Perfluorododecanoic acid-induced steroidogenic inhibition is associated with steroidogenic acute regulatory protein and reactive oxygen species in cAMP-stimulated Leydig cells. Toxicological Sciences 2010, 114:285-294.
37. Shi Z., Zhang H., Ding L., Feng Y., Wang J., Dai J. Proteomic analysis for testis of rats chronically exposed to perfluorododecanoic acid. Toxicology Letters 2010, 192:179-188.
38. Soung N.K., Park J.E., Yu L.R., Lee K.H., Lee J.M., Bang J.K., et al. Plk1-dependent and -independent roles of an ODF2 splice variant, hCenexin1, at the centrosome of somatic cells. Developmental Cell 2009, 16:539-550.
39. Tao L., Kannan K., Wong C.M., Arcaro K.F., Butenhoff J.L. Perfluorinated compounds in human milk from Massachusetts, U.S.A. Environmental Science and Technology 2008, 42:3096-3101.
40. Urner F., Sakkas D. Protein phosphorylation in mammalian spermatozoa. Reproduction 2003, 125:17-26.
41. Van de Vijver K.I., Holsbeek L., Das K., Blust R., Joiris C., De C.W. Occurrence of perfluorooctane sulfonate and other perfluorinated alkylated substances in harbor porpoises from the Black Sea. Environmental Science and Technology 2007, 41:315-320.
42. Viera A., Rufas J.S., Martinez I., Barbero J.L., Ortega S., Suja J.A. CDK2 is required for proper homologous pairing, recombination and sex-body formation during male mouse meiosis. Journal of Cell Science 2009, 122:2149-2159.
43. Woo R.A., Poon R.Y. Cyclin-dependent kinases and S phase control in mammalian cells. Cell Cycle 2003, 2:316-324.
44. Wu J., Shakey Q., Liu W., Schuller A., Follettie M.T. Global profiling of phosphopeptides by titania affinity enrichment. Journal of Proteome Research 2007, 6:4684-4689.
45. Yang Y., Sharma R., Cheng J.Z., Saini M.K., Ansari N.H., Andley U.P., et al. Protection of HLE B-3 cells against hydrogen peroxide- and naphthalene-induced lipid peroxidation and apoptosis by transfection with hGSTA1 and hGSTA2. Investigative Ophthalmology and Visual Science 2002, 43:434-445.