Phosphorylated AKT preserves stallion sperm viability and motility by inhibiting caspases 3 and 7

Reproduction

Volumn 148, Issue 2, 2014, Pages 221-235

  Gallardo Bolaños, Juan M ^a   Balao Da Silva, Carolina M ^a   Martín Muñoz, Patricia ^a   Morillo Rodríguez, Antolín ^a   Plaza Dávila, María ^a   Rodríguez Martínez, Heriberto ^c   Aparicio, Inés M ^b   Tapia, José A ^b   Ortega Ferrusola, Cristina ^a   Peña, Fernando J ^a  

^a Animal Production and Food Science Department Faculty of Veterinary Sciences   (Spain)

^b UNIVERSITY OF EXTREMADURA   (Spain)

^c LINKÖPING UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; CASPASE 7; PROTEIN KINASE B; REACTIVE OXYGEN METABOLITE;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; DEPHOSPHORYLATION; DNA FRAGMENTATION; EJACULATION; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME LOCALIZATION; ENZYME PHOSPHORYLATION; MALE; MALE GENITAL TRACT PARAMETERS; MITOCHONDRIAL MEMBRANE POTENTIAL; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SPERM PRESERVATION; SPERMATOZOON; SPERMATOZOON LIFESPAN; SPERMATOZOON MOTILITY; STALLION; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL CULTURE; CELL PROLIFERATION; CHEMISTRY; CYTOLOGY; ENZYME IMMUNOASSAY; FLOW CYTOMETRY; HORSE; METABOLISM; MITOCHONDRION; PHOSPHORYLATION; SEMEN ANALYSIS; WESTERN BLOTTING;

ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CASPASE 3; CASPASE 7; CELL PROLIFERATION; CELLS, CULTURED; FLOW CYTOMETRY; HORSES; IMMUNOENZYME TECHNIQUES; MALE; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; SEMEN ANALYSIS; SEMEN PRESERVATION; SPERM MOTILITY; SPERMATOZOA;

EID: 84903608415     PISSN: 14701626     EISSN: 17417899     Source Type: Journal    
DOI: 10.1530/REP-13-0191     Document Type: Article

References (59)

1. Aitken RJ & Koppers AJ 2011 Apoptosis and DNA damage in human spermatozoa. Asian Journal of Andrology 13 36-42. (doi:10.1038/aja.2010.68)
2. Aitken RJ, Findlay JK, Hutt KJ & Kerr JB 2011 Apoptosis in the germ line. Reproduction 141 139-150. (doi:10.1530/REP-10-0232)
3. Aitken RJ, De Iuliis GN, Gibb Z & Baker MA 2012 The simmet lecture: new horizons on an old landscape - oxidative stress, DNA damage and apoptosis in the male germ line. Reproduction in Domestic Animals 47 (Suppl 4) 7-14. (doi:10.1111/j.1439-0531.2012.02049.x)
4. Aparicio IM, Gil MC, Garcia-Herreros M, Pena FJ & Garcia-Marin LJ 2005 Inhibition of phosphatidylinositol 3-kinase modifies boar sperm motion parameters. Reproduction 129 283-289. (doi:10.1530/rep.1.00447) (Pubitemid 40425638)
5. Aquila S, Middea E, Catalano S, Marsico S, Lanzino M, Casaburi I, Barone I, Bruno R, Zupo S & Ando S 2007 Human sperm express a functional androgen receptor: effects on PI3K/AKT pathway. Human Reproduction 22 2594-2605. (doi:10.1093/humrep/dem243) (Pubitemid 47439671)
6. Balao da Silva CM, Ortega Ferrusola C, Morillo Rodriguez A, Gallardo Bolanos JM, Plaza Davila M, Morrell JM, Rodriguez Martinez H, Tapia JA, Aparicio IM & Pena FJ 2013 Sex sorting increases the permeability of the membrane of stallion spermatozoa. Animal Reproduction Science 138 241-251. (doi:10.1016/j.anireprosci.2013. 02.021)
7. Ball BA 2008 Oxidative stress, osmotic stress and apoptosis: impacts on sperm function and preservation in the horse. Animal Reproduction Science 107 257-267. (doi:10.1016/j.anireprosci.2008.04.014)
8. Baumgarth N & Roederer M 2000 A practical approach to multicolor flow cytometry for immunophenotyping. Journal of Immunological Methods 243 77-79. (doi:10.1016/S0022-1759(00)00229-5)
9. Busch F, Mobasheri A, Shayan P, Lueders C, Stahlmann R & Shakibaei M 2012 Resveratrolmodulates interleukin-1b-induced phosphatidylinositol 3-kinase and nuclear factor κB signaling pathways in human tenocytes. Journal of Biological Chemistry 287 38050-38063. (doi:10.1074/jbc.M112.377028)
10. Chekeni FB, Elliott MR, Sandilos JK, Walk SF, Kinchen JM, Lazarowski ER, Armstrong AJ, Penuela S, Laird DW, Salvesen GS et al. 2010 Pannexin 1 channels mediate 'find-me' signal release and membrane permeability during apoptosis. Nature 467 863-867. (doi:10.1038/nature09413)
11. De Iuliis GN, Thomson LK, Mitchell LA, Finnie JM, Koppers AJ, Hedges A, Nixon B & Aitken RJ 2009 DNA damage in human spermatozoa is highly correlated with the efficiency of chromatin remodeling and the formation of 8-hydroxy-20-deoxyguanosine, a marker of oxidative stress. Biology of Reproduction 81 517-524. (doi:10.1095/biolreprod.109.076836)
12. Elliott MR, Chekeni FB, Trampont PC, Lazarowski ER, Kadl A, Walk SF, Park D, Woodson RI, Ostankovich M, Sharma P et al. 2009 Nucleotides released by apoptotic cells act as a find-me signal to promote phagocytic clearance. Nature 461 282-286. (doi:10.1038/nature08296)
13. Garcia BM, Fernandez LG, Ferrusola CO, Salazar-Sandoval C, Rodriguez AM, Martinez HR, Tapia JA, Morcuende D & Pena FJ 2011 Membrane lipids of the stallion spermatozoon in relation to sperm quality and susceptibility to lipid peroxidation. Reproduction in Domestic Animals 46 141-148. (doi:10.1111/j.1439- 0531.2010.01609.x)
14. Gilot D, Giudicelli F, Lagadic-Gossmann D & Fardel O 2010 AKTi-1/2, an allosteric inhibitor of AKT 1 and 2, efficiently inhibits CaMKIa activity and aryl hydrocarbon receptor pathway. Chemico-Biological Interactions 188 546-552. (doi:10.1016/j.cbi.2010.08.011)
15. Gonzalez-Fernandez L, Ortega-Ferrusola C, Macias-Garcia B, Salido GM, Pena FJ & Tapia JA 2009 Identification of protein tyrosine phosphatases and dual-specificity phosphatases in mammalian spermatozoa and their role in sperm motility and protein tyrosine phosphorylation. Biology of Reproduction 80 1239-1252. (doi:10.1095/biolreprod.108.073486)
16. Hers I, Vincent EE & Tavare JM 2011 AKT signalling in health and disease. Cellular Signalling 23 1515-1527. (doi:10.1016/j.cellsig.2011.05.004)
17. Koppers AJ, De Iuliis GN, Finnie JM, McLaughlin EA & Aitken RJ 2008 Significance of mitochondrial reactive oxygen species in the generation of oxidative stress in spermatozoa. Journal of Clinical Endocrinology and Metabolism 93 3199-3207. (doi:10.1210/jc.2007-2616)
18. Koppers AJ, Mitchell LA,Wang P, Lin M& Aitken RJ 2011 Phosphoinositide 3-kinase signalling pathway involvement in a truncated apoptotic cascade associated with motility loss and oxidative DNA damage in human spermatozoa. Biochemical Journal 436 687-698. (doi:10.1042/ BJ20110114)
19. Krutzik PO, Irish JM, Nolan GP & Perez OD 2004 Analysis of protein phosphorylation and cellular signaling events by flow cytometry: techniques and clinical applications. Clinical Immunology 110 206-221. (doi:10.1016/j.clim. 2003.11.009) (Pubitemid 38402001)
20. Lan TH, Xu ZW,Wang Z,Wu YL,Wu WK & Tan HM 2011 Ginsenoside Rb1 prevents homocysteine-induced endothelial dysfunction via PI3K/AKT activation and PKC inhibition. Biochemical Pharmacology 82 148-155. (doi:10.1016/j.bcp. 2011.04.001)
21. Lessig J, Spalteholz H, Reibetanz U, Salavei P, Fischlechner M, Glander HJ & Arnhold J 2007 Myeloperoxidase binds to non-vital spermatozoa on phosphatidylserine epitopes. Apoptosis 12 1803-1812. (doi:10.1007/s10495-007- 0113-5) (Pubitemid 47498248)
22. Luconi M, Marra F, Gandini L, Filimberti E, Lenzi A, Forti G & Baldi E 2001 Phosphatidylinositol 3-kinase inhibition enhances human sperm motility. Human Reproduction 16 1931-1937. (doi:10.1093/humrep/16.9.1931) (Pubitemid 32916224)
23. Luconi M, Torcia S, Grillo D, Fiorenza MT, Forti G, Mangia F & Baldi E 2005 Enhancement of mouse sperm motility by the PI3-kinase inhibitor LY294002 does not result in toxic effects on preimplantation embryo development. Human Reproduction 20 3500-3504. (doi:10.1093/humrep/dei248) (Pubitemid 41742533)
24. Macías Garcia B, Gonzalez Fernandez L, Ortega Ferrusola C, Morillo Rodriguez A, Gallardo Bolanos JM, Rodriguez Martinez H, Tapia JA, Morcuende D & Pena FJ 2011a Fatty acids and plasmalogens of the phospholipids of the sperm membranes and their relation with the postthaw quality of stallion spermatozoa. Theriogenology 75 811-818. (doi:10.1016/j.theriogenology.2010.10. 021)
25. Macías Garcia B, Miro Moran A, Gonzalez Fernandez L, Ortega Ferrusola C, Morillo Rodriguez A, Gallardo Bolaños JM, Balao da Silva CM, Rodriguez Martinez H & Peña FJ 2011b The mitochondria of stallion spermatozoa are more sensitive than the plasmalemma to osmotic induced stress: role of the c Jun terminal kinase (JMK) pathway. Journal of Andrology 33 105-113. (doi:10.2164/jandrol.110.011957)
26. Macías Garcia B, Ortega Ferrusola C, Aparicio IM, Miro-Moran A, Morillo Rodriguez A, Gallardo Bolanos JM, Gonzalez Fernandez L, Balao da Silva CM, RodriguezMartinezH, Tapia JAet al. 2012 Toxicity of glycerol for the stallion spermatozoa: effects on membrane integrity and cytoskeleton, lipid peroxidation and mitochondrial membrane potential. Theriogenology 77 1280-1289. (doi:10.1016/j.theriogenology.2011.10.033)
27. Martínez-Pastor F, Jorge Tizado E, Garde JJ, Anel L & de Paz P 2011 Opportunities and challenges of sperm motility subpopulation analysis. Theriogenology 75 783-795. (doi:10.1016/j.theriogenology.2010.11. 034)
28. Mendoza N, Casao A, Perez-Pe R, Cebrian-Perez JA & Muino-Blanco T 2013 New insights into the mechanisms of ram sperm protection by seminal plasma proteins. Biology of Reproduction 88 149. (doi:10.1095/biolreprod.112.105650)
29. Moran JM, Madejon L, Ortega Ferrusola C & Peña FJ 2008 Nitric oxide induces caspase activity in boar spermatozoa. Theriogenology 70 91-96. (doi:10.1016/j.theriogenology.2008.02.010)
30. Nauc V, De Lamirande E, Leclerc P & Gagnon C 2004 Inhibitors of phosphoinositide 3-kinase, LY294002 and Wortmannin, affect sperm capacitation and associated phosphorylation of proteins differently: Ca2C-dependent divergences. Journal of Andrology 25 573-585. (doi:10.1002/j.1939-4640.2004. tb02828.x) (Pubitemid 38880192)
31. Nuñez-Martinez I, Moran JM & Peña FJ 2007a Identification of sperm morphometric subpopulations in the canine ejaculate: do they reflect different subpopulations in sperm chromatin integrity? Zygote 15 257-266. (doi:10.1017/S0967199407004248) (Pubitemid 47117316)
32. Nuñez-Martinez I, Moran JM & Peña FJ 2007b Sperm indexes obtained using computer-assisted morphometry provide a forecast of the freezability of canine sperm. International Journal of Andrology 30 182-189. (doi:10.1111/j.1365-2605.2007.00743.x) (Pubitemid 46802108)
33. Ortega-Ferrusola C, Sotillo-Galan Y, Varela-Fernandez E, Gallardo- Bolanos JM, Muriel A, Gonzalez-Fernandez L, Tapia JA & Peña FJ 2008 Detection of "apoptosis-like" changes during the cryopreservation process in equine sperm. Journal of Andrology 29 213-221. (doi:10.2164/jandrol. 107.003640) (Pubitemid 351345719)
34. Ortega Ferrusola C, Gonzalez Fernandez L, Macias Garcia B, Salazar- Sandoval C, Morillo Rodriguez A, Rodriguez Martinez H, Tapia JA & Peña FJ 2009a Effect of cryopreservation on nitric oxide production by stallion spermatozoa. Biology of Reproduction 81 1106-1111. (doi:10.1095/biolreprod.109. 078220)
35. Ortega Ferrusola C, Garcia BM, Gallardo-Bolanos JM, Gonzalez- Fernandez L, Rodriguez-Martinez H, Tapia JA & Peña FJ 2009b Lipid peroxidation, assesed with BODIPY-C11, increases after cryopreservation of stallion spermatozoa, is stallion-dependent and is related to apoptotic-like changes. Reproduction 138 55-63. (doi:10.1530/REP-08-0484)
36. Ortega-Ferrusola C, Garcia BM, Gallardo-Bolanos JM, Gonzalez- Fernandez L, Rodriguez-Martinez H, Tapia JA & Peña FJ 2009c Apoptotic markers can be used to forecast the freezeability of stallion spermatozoa. Animal Reproduction Science 114 393-403. (doi:10.1016/j.anireprosci.2008.10.005)
37. Ortega Ferrusola C, Gonzalez Fernandez L, Salazar Sandoval C, Macias Garcia B, Rodriguez Martinez H, Tapia JA & Peña FJ 2010 Inhibition of the mitochondrial permeability transition pore reduces "apoptosis like" changes during cryopreservation of stallion spermatozoa. Theriogenology 74 458-465. (doi:10.1016/j.theriogenology.2010.02.029)
38. Parte PP, Rao P, Redij S, Lobo V, D'Souza SJ, Gajbhiye R & Kulkarni V 2012 Sperm phosphoproteome profiling by ultra performance liquid chromatography followed by data independent analysis (LC-MS(E)) reveals altered proteomic signatures in asthenozoospermia. Journal of Proteomics 75 5861-5871. (doi:10.1016/j.jprot.2012.07.003)
39. Peña FJ, Johannisson A, Wallgren M & Rodriguez-Martinez H 2003a Assessment of fresh and frozen-thawed boar semen using an Annexin-V assay: a new method of evaluating sperm membrane integrity. Theriogenology 60 677-689. (doi:10.1016/S0093-691X(03)00081-5) (Pubitemid 36914705)
40. Peña FJ, Johannisson A, Wallgren M & Rodriguez Martinez H 2003b Antioxidant supplementation in vitro improves boar sperm motility and mitochondrial membrane potential after cryopreservation of different fractions of the ejaculate. Animal Reproduction Science 78 85-98. (doi:10.1016/S0378- 4320(03)00049-6) (Pubitemid 37042010)
41. Peña FJ, Saravia F, Garcia-Herreros M, Nuñez-martinez I, Tapia JA, Johannisson A, Wallgren M & Rodriguez-Martinez H 2005a Identification of sperm morphometric subpopulations in two different portions of the boar ejaculate and its relation to postthaw quality. Journal of Andrology 26 716-723. (doi:10.2164/jandrol.05030) (Pubitemid 41476630)
42. Peña FJ, Saravia F, Johannisson A, Walgren M & Rodriguez-Martinez H 2005b A new and simple method to evaluate early membrane changes in frozen-thawed boar spermatozoa. International Journal of Andrology 28 107-114. (doi:10.1111/j.1365-2605.2005.00512.x) (Pubitemid 40461181)
43. Peña FJ, Nuñez-Martinez I & Moran JM 2006 Semen technologies in dog breeding: an update. Reproduction in Domestic Animals 41 (Suppl 2) 21-29. (doi:10.1111/j.1439-0531.2006.00766.x) (Pubitemid 44370106)
44. Peña FJ, Ortega-Ferrusola C, Tapia JA & Aparicio IM 2012 How stallion sperm age in vitro? Scenario for preservation technologies Journal of Equine Veterinary Science 32 451-454. (doi:10.1016/j.jevs.2012.05.074)
45. Petrunkina AM & Harrison RA 2011 Mathematical analysis of misestimation of cell subsets in flow cytometry: viability staining revisited. Journal of Immunological Methods 368 71-79. (doi:10.1016/j.jim.2011.02.009)
46. du Plessis SS, Franken DR, Baldi E & Luconi M 2004 Phosphatidylinositol 3-kinase inhibition enhances human sperm motility and sperm-zona pellucida binding. International Journal of Andrology 27 19-26. (doi:10.1111/j.1365-2605.2004.00440.x) (Pubitemid 38177926)
47. PujiantoDA, Curry BJ&Aitken RJ 2010 Prolactin exerts a prosurvival effect on human spermatozoa via mechanisms that involve the stimulation of AKT phosphorylation and suppression of caspase activation and capacitation. Endocrinology 151 1269-1279. (doi:10.1210/en.2009-0964)
48. Qiao Q, Jiang Y & Li G 2013 Inhibition of the PI3K/AKT-NF-κB pathway with curcumin enhanced radiation-induced apoptosis in human Burkitt's lymphoma. Journal of Pharmacological Sciences 121 247-256. (doi:10.1254/jphs. 12149FP)
49. Roederer M 2001 Spectral compensation for flow cytometry: visualization artifacts, limitations and caveats. Cytometry 45 194-205. (doi:10.1002/1097- 0320(20011101)45:3〈194::AID-CYTO1163〉3.0.CO;2-C) (Pubitemid 33064141)
50. Said TM, Gaglani A & Agarwal A 2010 Implication of apoptosis in sperm cryoinjury. Reproductive Biomedicine Online 21 456-462. (doi:10.1016/j.rbmo. 2010.05.011)
51. Sakkas D, Moffatt O, Manicardi GC, Mariethoz E, Tarozzi N & Bizzaro D 2002 Nature of DNA damage in ejaculated human spermatozoa and the possible involvement of apoptosis. Biology of Reproduction 66 1061-1067. (doi:10.1095/biolreprod66.4.1061) (Pubitemid 34263125)
52. Sandilos JK, Chiu YH, Chekeni FB, Armstrong AJ, Walk SF, Ravichandran KS & Bayliss DA 2012 Pannexin 1, an ATP release channel, is activated by caspase cleavage of its pore-associated C-terminal autoinhibitory region. Journal of Biological Chemistry 287 11303-11311. (doi:10.1074/jbc.M111.323378)
53. Schulz KR, Danna EA, Krutzik PO & Nolan GP 2007 Single-cell phosphoprotein analysis by flow cytometry. In Current Protocols in Immunology, ch 8, unit 8 17. Ed John E Coligan et al. Wiley Blackwell, NJ, USA
54. Schulz KR, Danna EA, Krutzik PO & Nolan GP 2012 Single-cell phosphoprotein analysis by flowcytometry. In Current Protocols in Immunology, ch 8, unit 8 17, pp 11-20. Ed John E Coligan et al.Wiley Blackwell, NJ USA
55. Sethi G, Ahn KS, Sung B, Kunnumakkara AB, Chaturvedi MM & Aggarwal BB 2008 SH-5, an AKT inhibitor potentiates apoptosis and inhibits invasion through the suppression of anti-apoptotic, proliferative and metastatic gene products regulated by IκBa kinase activation. Biochemical Pharmacology 76 1404-1416. (doi:10.1016/j.bcp.2008.05.023)
56. Shimokawa K, Oshiro R, Yamanaka K, Ashizawa K, Ohta S & Tatemoto H 2012 Improvement of the post-thaw qualities of Okinawan native Agu pig sperm frozen in an extender supplemented with antiapoptotic PTD-FNK protein. Theriogenology 78 1446-1455. (doi:10.1016/j.theriogenology.2012.06.005)
57. da Silva CM, Macias-Garcia B, Miro-Moran A, Gonzalez-Fernandez L, Morillo-Rodriguez A, Ortega-Ferrusola C, Gallardo-Bolanos JM, Stilwell G, Tapia JA & Pena FJ 2011 Melatonin reduces lipid peroxidation and apoptotic-like changes in stallion spermatozoa. Journal of Pineal Research 51 172-179. (doi:10.1111/j.1600-079X.2011.00873.x)
58. Tazzari PL, Cappellini A, Bortul R, Ricci F, Billi AM, Tabellini G, Conte R & Martelli AM 2002 Flow cytometric detection of total and serine 473 phosphorylated AKT. Journal of Cellular Biochemistry 86 704-715. (doi:10.1002/jcb.10262) (Pubitemid 34839972)
59. Yang CM, Lee IT, Lin CC, Wang CH, Cherng WJ & Hsiao LD 2013 c-Src-dependent MAPKs/AP-1 activation is involved in TNF-a-induced matrix metalloproteinase-9 expression in rat heart-derived H9c2 cells. Biochemical Pharmacology 85 1115-1123. (doi:10.1016/j.bcp.2013.01.013)