AMP-activated kinase, AMPK, is involved in the maintenance of plasma membrane organization in boar spermatozoa

Biochimica et Biophysica Acta - Biomembranes

Volumn 1828, Issue 9, 2013, Pages 2143-2151

  Hurtado De Llera, Ana ^a   Martin Hidalgo, David ^a   Rodriguez Gil, Joan E ^b   Gil, M Cruz ^a   Garcia Marin, Luis J ^a   Bragado, M Julia ^a  

^a UNIVERSITY OF EXTREMADURA   (Spain)

^b UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

Author keywords

Acrosome membrane; AMPK; Lipid disorganization; Phosphatidylserine externalization; Spermatozoa plasmalemma

Indexed keywords

8 BROMO CYCLIC AMP; CALCIMYCIN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; MEMBRANE LIPID; PHOSPHATIDYLSERINE; PHOSPHOTRANSFERASE INHIBITOR; (6 (4 (2 PIPERIDIN 1 YLETHOXY)PHENYL)) 3 PYRIDIN 4 YLPYRAZOLO(1,5 A)PYRIMIDINE; (6-(4-(2-PIPERIDIN-1-YLETHOXY)PHENYL))-3-PYRIDIN-4-YLPYRAZOLO(1,5-A)PYRIMIDINE; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; ISOENZYME; PYRAZOLE DERIVATIVE; PYRIMIDINE DERIVATIVE;

ACROSOME REACTION; ANIMAL CELL; ARTICLE; CELL AGGREGATION; CELL MEMBRANE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; FLOW CYTOMETRY; IMMUNOFLUORESCENCE; INCUBATION TIME; MALE; MEMBRANE TRANSPORT; MITOCHONDRIAL MEMBRANE POTENTIAL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPERMATOZOON; SPERMATOZOON MIDPIECE; SPERMATOZOON TAIL; SWINE; WESTERN BLOTTING; ACROSOME; ACROSOME MEMBRANE; AMPK; ANIMAL; DRUG EFFECT; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; LIPID DISORGANIZATION; METABOLISM; MITOCHONDRION; PHOSPHATIDYLSERINE EXTERNALIZATION; PHOSPHORYLATION; SIGNAL TRANSDUCTION; SPERMATOZOA PLASMALEMMA; SPERMATOZOON CAPACITATION; SPERMATOZOON MOTILITY; ULTRASTRUCTURE;

MAMMALIA;

ACROSOME MEMBRANE; AMPK; LIPID DISORGANIZATION; PHOSPHATIDYLSERINE EXTERNALIZATION; SPERMATOZOA PLASMALEMMA;

8-BROMO CYCLIC ADENOSINE MONOPHOSPHATE; ACROSOME; ACROSOME REACTION; AMP-ACTIVATED PROTEIN KINASES; ANIMALS; CALCIMYCIN; CELL MEMBRANE; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; GENE EXPRESSION REGULATION; ISOENZYMES; MALE; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; PHOSPHORYLATION; PYRAZOLES; PYRIMIDINES; SIGNAL TRANSDUCTION; SPERM CAPACITATION; SPERM MOTILITY; SWINE;

EID: 84879215933     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2013.05.026     Document Type: Article

References (45)

1. R. Yanagimachi Mammalian fertilization E. Knobil, J.D. Neil, The Physiology of Reproduction 1994 Raven press New York 189 317
2. Y. Gur, and H. Breitbart Mammalian sperm translate nuclear-encoded proteins by mitochondrial-type ribosomes Genes Dev. 20 4 2006 411 416 (Pubitemid 43244394)
3. O. Hernandez-Perez, G. Luna, and A. Reyes Re-evaluation of the role of spermatozoa as inducers of protein synthesis by the rabbit endometrium Arch. Androl. 11 3 1983 239 243 (Pubitemid 14213627)
4. M.A. Baker, L. Hetherington, H. Ecroyd, S.D. Roman, and R.J. Aitken Analysis of the mechanism by which calcium negatively regulates the tyrosine phosphorylation cascade associated with sperm capacitation J. Cell Sci. 117 Pt 2 2004 211 222 (Pubitemid 38128900)
5. M.M. Bravo, I.M. Aparicio, M. Garcia-Herreros, M.C. Gil, F.J. Pena, and L.J. Garcia-Marin Changes in tyrosine phosphorylation associated with true capacitation and capacitation-like state in boar spermatozoa Mol. Reprod. Dev. 71 1 2005 88 96 (Pubitemid 40471809)
6. P.E. Visconti, J.L. Bailey, G.D. Moore, D. Pan, P. Olds-Clarke, and G.S. Kopf Capacitation of mouse spermatozoa. I. Correlation between the capacitation state and protein tyrosine phosphorylation Development 121 4 1995 1129 1137
7. D. Krapf, E. Arcelay, E.V. Wertheimer, A. Sanjay, S.H. Pilder, A.M. Salicioni, and P.E. Visconti Inhibition of Ser/Thr phosphatases induces capacitation-associated signaling in the presence of Src kinase inhibitors J. Biol. Chem. 285 11 2010 7977 7985
8. L.J. Garrett, S.G. Revell, and H.J. Leese Adenosine triphosphate production by bovine spermatozoa and its relationship to semen fertilizing ability J. Androl. 29 4 2008 449 458 (Pubitemid 351929930)
9. K. Miki Energy metabolism and sperm function Soc. Reprod. Fertil. Suppl. 65 309-25 2007 309 325
10. D.G. Hardie, S.A. Hawley, and J.W. Scott AMP-activated protein kinase - development of the energy sensor concept J. Physiol. 574 Pt 1 2006 7 15 (Pubitemid 43905792)
11. Y.C. Long, and J.R. Zierath AMP-activated protein kinase signaling in metabolic regulation J. Clin. Invest. 116 7 2006 1776 1783 (Pubitemid 44033297)
12. D. Carling AMPK Curr. Biol. 14 6 2004 R220
13. B.B. Kahn, T. Alquier, D. Carling, and D.G. Hardie AMP-activated protein kinase: ancient energy gauge provides clues to modern understanding of metabolism Cell Metab. 1 1 2005 15 25 (Pubitemid 43960587)
14. D.G. Hardie AMP-activated protein kinase: an energy sensor that regulates all aspects of cell function Genes Dev. 25 18 2011 1895 1908
15. D.G. Hardie AMP-activated protein kinase R. Bradshaw, E. Dennis, Handbook of Cell Signaling Second ed. 2010 Elsevier 551 556
16. A. Hurtado de Llera, D. Martin-Hidalgo, M.C. Gil, L.J. Garcia-Marin, and M.J. Bragado AMP-activated kinase AMPK is expressed in boar spermatozoa and regulates motility PLoS One 7 6 2012 e38840
17. M.C. Towler, S. Fogarty, S.A. Hawley, D.A. Pan, D.M. Martin, N.A. Morrice, A. McCarthy, M.N. Galardo, S.B. Meroni, S.B. Cigorraga, A. Ashworth, K. Sakamoto, and D.G. Hardie A novel short splice variant of the tumour suppressor LKB1 is required for spermiogenesis Biochem. J. 416 1 2008 1 14
18. B. Xu, Z. Hao, K.N. Jha, Z. Zhang, C. Urekar, L. Digilio, S. Pulido, J.F. Strauss 3rd, C.J. Flickinger, and J.C. Herr Targeted deletion of Tssk1 and 2 causes male infertility due to haploinsufficiency Dev. Biol. 319 2 2008 211 222
19. B. Xu, Z. Hao, K.N. Jha, L. Digilio, C. Urekar, Y.H. Kim, S. Pulido, C.J. Flickinger, and J.C. Herr Validation of a testis specific serine/threonine kinase [TSSK] family and the substrate of TSSK1 & 2, TSKS, as contraceptive targets Soc. Reprod. Fertil. Suppl. 63 2007 87 101
20. A.R. Ramirez, M.A. Castro, C. Angulo, L. Ramio, M.M. Rivera, M. Torres, T. Rigau, J.E. Rodriguez-Gil, and Ll. Concha The presence and function of dopamine type 2 receptors in boar sperm: a possible role for dopamine in viability, capacitation, and modulation of sperm motility Biol. Reprod. 80 4 2009 753 761
21. D. Martin-Hidalgo, F.J. Baron, M.J. Bragado, P. Carmona, A. Robina, L.J. Garcia-Marin, and M.C. Gil The effect of melatonin on the quality of extended boar semen after long-term storage at 17 C Theriogenology 75 8 2011 1550 1560
22. K.E. Waterhouse, P.M. De Angelis, T. Haugan, H. Paulenz, P.O. Hofmo, and W. Farstad Effects of in vitro storage time and semen-extender on membrane quality of boar sperm assessed by flow cytometry Theriogenology 62 9 2004 1638 1651 (Pubitemid 39415753)
23. D.G. Hardie The AMP-activated protein kinase pathway - new players upstream and downstream J. Cell Sci. 117 Pt 23 2004 5479 5487 (Pubitemid 40012195)
24. G. Martin, O. Sabido, P. Durand, and R. Levy Phosphatidylserine externalization in human sperm induced by calcium ionophore A23187: relationship with apoptosis, membrane scrambling and the acrosome reaction Hum. Reprod. 20 12 2005 3459 3468 (Pubitemid 41742528)
25. C. Voisine, E.A. Craig, N. Zufall, A.O. von, N. Pfanner, and W. Voos The protein import motor of mitochondria: unfolding and trapping of preproteins are distinct and separable functions of matrix Hsp70 Cell 97 5 1999 565 574 (Pubitemid 29256960)
26. B.M. Acton, A. Jurisicova, I. Jurisica, and R.F. Casper Alterations in mitochondrial membrane potential during preimplantation stages of mouse and human embryo development Mol. Hum. Reprod. 10 1 2004 23 32 (Pubitemid 38195962)
27. H.D. Guthrie, and G.R. Welch Impact of storage prior to cryopreservation on plasma membrane function and fertility of boar sperm Theriogenology 63 2 2005 396 410 (Pubitemid 40033964)
28. R. Rathi, B. Colenbrander, M.M. Bevers, and B.M. Gadella Evaluation of in vitro capacitation of stallion spermatozoa Biol. Reprod. 65 2 2001 462 470 (Pubitemid 32702310)
29. C.E. Green, and P.F. Watson Comparison of the capacitation-like state of cooled boar spermatozoa with true capacitation Reproduction 122 6 2001 889 898 (Pubitemid 33138569)
30. B.M. Gadella, and R.A. Harrison The capacitating agent bicarbonate induces protein kinase A-dependent changes in phospholipid transbilayer behavior in the sperm plasma membrane Development 127 11 2000 2407 2420 (Pubitemid 30386579)
31. L. Vucicevic, M. Misirkic, K. Janjetovic, L. Harhaji-Trajkovic, M. Prica, D. Stevanovic, E. Isenovic, E. Sudar, M. Sumarac-Dumanovic, D. Micic, and V. Trajkovic AMP-activated protein kinase-dependent and -independent mechanisms underlying in vitro antiglioma action of compound C Biochem. Pharmacol. 77 11 2009 1684 1693
32. C. Zelenak, M. Föller, A. Velic, K. Krug, S.M. Qadri, B. Viollet, F. Lang, and B. Macek Proteome analysis of erythrocytes lacking AMP-activated protein kinase reveals a role of PAK2 kinase in eryptosis J. Proteome Res. 10 4 2011 1690 1697
33. H. Harayama Viability and protein phosphorylation patterns of boar spermatozoa agglutinated by treatment with a cell-permeable cyclic adenosine 3′,5′-monophosphate analog J. Androl. 24 6 2003 831 842 (Pubitemid 37370539)
34. R.A. Harrison Capacitation mechanisms, and the role of capacitation as seen in eutherian mammals Reprod. Fertil. Dev. 8 4 1996 581 594 (Pubitemid 26288033)
35. Y. Gao, Y. Zhou, A. Xu, and D. Wu Effects of an AMP-activated protein kinase inhibitor, compound C, on adipogenic differentiation of 3T3-L1 cells Biol. Pharm. Bull. 31 9 2008 1716 1722
36. C.B. Favero, and J.W. Mandell A pharmacological activator of AMP-activated protein kinase (AMPK) induces astrocyte stellation Brain Res. 116 8 2007 1 10 (Pubitemid 47320626)
37. F.M. Flesch, and B.M. Gadella Dynamics of the mammalian sperm plasma membrane in the process of fertilization Biochim. Biophys. Acta 1469 3 2000 197 235
38. P.S. James, C.A. Wolfe, S. Ladha, and R. Jones Lipid diffusion in the plasma membrane of ram and boar spermatozoa during maturation in the epididymis measured by fluorescence recovery after photobleaching Mol. Reprod. Dev. 52 2 1999 207 215 (Pubitemid 29013390)
39. B.M. Gadella, P.S. Tsai, A. Boerke, and I.A. Brewis Sperm head membrane reorganisation during capacitation Int. J. Dev. Biol. 52 5-6 2008 473 480
40. R.A. Schlegel, M. Stevens, K. Lumley-Sapanski, and P. Williamson Altered lipid packing identifies apoptotic thymocytes Immunol. Lett. 36 3 1993 283 288 (Pubitemid 23214535)
41. G. Koopman, C.P. Reutelingsperger, G.A. Kuijten, R.M. Keehnen, S.T. Pals, and M.H. van Oers Annexin V for flow cytometric detection of phosphatidylserine expression on B cells undergoing apoptosis Blood 84 5 1994 1415 1420 (Pubitemid 24273007)
42. I. Vermes, C. Haanen, H. Steffens-Nakken, and C. Reutelingsperger A novel assay for apoptosis. Flow cytometric detection of phosphatidylserine expression on early apoptotic cells using fluorescein labelled Annexin V J. Immunol. Methods 184 1 1995 39 51
43. F.M. Flesch, J.F. Brouwers, P.F. Nievelstein, A.J. Verkleij, L.M. van Golde, B. Colenbrander, and B.M. Gadella Bicarbonate stimulated phospholipid scrambling induces cholesterol redistribution and enables cholesterol depletion in the sperm plasma membrane J. Cell Sci. 114 19 2001 3543 3555 (Pubitemid 33019770)
44. G.P. Sapkota, A. Kieloch, J.M. Lizcano, S. Lain, J.S. Arthur, M.R. Williams, N. Morrice, M. Deak, and D.R. Alessi Phosphorylation of the protein kinase mutated in Peutz-Jeghers cancer syndrome, LKB1/STK11, at Ser431 by p90(RSK) and cAMP-dependent protein kinase, but not its farnesylation at Cys(433), is essential for LKB1 to suppress cell vrowth J. Biol. Chem. 276 22 2001 19469 19482
45. N. Djouder, R.D. Tuerk, M. Suter, P. Salvioni, R.F. Thali, R. Scholz, K. Vaahtomeri, Y. Auchli, H. Rechsteiner, R.A. Brunisholz, B. Viollet, T.P. Mäkelä, T. Wallimann, D. Neumann, and W. Krek PKA phosphorylates and inactivates AMPKalpha to promote efficient lipolysis EMBO J. 29 2 2010 469 481