Muscle glycogen synthase isoform is responsible for testicular glycogen synthesis: Glycogen overproduction induces apoptosis in male germ cells

Journal of Cellular Biochemistry

Volumn 114, Issue 7, 2013, Pages 1653-1664

  Villarroel Espíndola, Franz ^a   Maldonado, Rodrigo ^a   Mancilla, Héctor ^a   Vander Stelt, Karen ^a   Acuña, Aníbal I ^a   Covarrubias, Alejandra ^a   Lõpez, Camila ^a   Angulo, Constanza ^a   Castro, Maite A ^a   Slebe, Juan Carlos ^a   Durán, Jordi ^b   García Rocha, Mar ^b   Guinovart, Joan J ^c   Concha, Ilona I ^a  

^a UNIVERSIDAD AUSTRAL DE CHILE   (Chile)

^b INSTITUTE FOR RESEARCH IN BIOMEDICINE   (Spain)

^c UNIVERSITY OF BARCELONA   (Spain)

Author keywords

APOPTOSIS; GLYCOGEN; GLYCOGEN SYNTHASE; SEMINIFEROUS TUBULES; TESTIS

Indexed keywords

CASPASE 3; ENZYME; GLYCOGEN SYNTHASE; LAFORIN; MALIN; MUSCLE GLYCOGEN SYNTHASE; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; ENZYME ACTIVATION; ENZYME ACTIVITY; GERM CELL; GLYCOGEN SYNTHESIS; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SERTOLI CELL; TESTIS; UBIQUITINATION;

ANIMALS; APOPTOSIS; GERM CELLS; GLYCOGEN; GLYCOGEN SYNTHASE; IMMUNOBLOTTING; MALE; MICE; MICE, TRANSGENIC; PROTEIN ISOFORMS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEMINIFEROUS TUBULES; TESTIS;

EID: 84877704456     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.24507     Document Type: Article

References (50)

1. Amann RP,. 2008. The cycle of the seminiferous epithelium in humans: A need to revisit ? J Androl 29 (5): 469-487.
2. Angulo C, Castro MA, Rivas CI, Segretain D, Maldonado R, Yañez AJ, Slebe JC, Vera JC, Concha II,. 2008. Molecular identification and functional characterization of the vitamin C transporters expressed by Sertoli cells. J Cell Physiol 217 (3): 708-716.
3. Angulo C, Maldonado R, Pulgar E, Mancilla H, Cõrdova A, Villarroel F, Castro MA, Concha II,. 2011. Vitamin C and oxidative stress in the seminiferous epithelium. Biol Research 44: 169-180.
4. Arzac JP,. 1950. Glycogen in human testicular biopsy material. J Clin Endocrinol Metab 10 (11): 1465-1470.
5. Arzac JP,. 1953. Physiological function of human testicular glycogen: A tentative theory. Ann Ostet Ginecol 75 (6): 804-818.
6. Austin CR, Short RV,. 1972. Reproduction in mammals, book 1 Germ cells and fertilization. New York (NY, USA): Cambridge University Press.
7. Ballester J, Fernández-Novell JM, Rutllant J, García-Rocha M, Palomo MJ, Mogas T, Peña A, Rigau T, Guinovart JJ, Rodriguez-Gil JE,. 2000. Evidence for a functional glycogen metabolism in mature mammalian spermatozoa. Mol Reprod Dev 56: 207-219. (Pubitemid 30252707)
8. Bourdon V, Lablack A, Abbe P, Segretain D, Pointis G,. 1998. Characterization of a clonal sertoli cell line using adult PyLT transgenic mice. Biol Reprod 58: 591-599. (Pubitemid 28099128)
9. Browner MF, Nakano K, Bang AG, Fletterick RJ,. 1989. Human muscle glycogen synthase cDNA sequence: A negatively charged protein with an asymmetric charge distribution. Proc Natl Acad Sci USA 86: 1443-1447. (Pubitemid 19078925)
10. Cavanagh JB,. 1999. Corpora-amylacea and the family of polyglucosan diseases. Brain Res Rev 29: 265-295. (Pubitemid 29191343)
11. Datta K, Misra J, Dasgupta T, Sengupta S, Sengupta DE,. 1988. Glycogen metabolism in human fetal testes. J Biosci 13 (2): 117-121.
12. Duran J, Tevy MF, Garcia-Rocha M, Calbõ J, Milán M, Guinovart JJ,. 2012. Deleterious effects of neuronal accumulation of glycogen in flies and mice. EMBO Mol Med 4: 1-11.
13. Ewing LL, Means AR, Beames CG, Montgomery RD,. 1966. Biochemical changes in rat testis during postnatal maturation. J Reprod Fert 12: 295-307.
14. Fabbrini A, Re M, Conti C,. 1969. Glycogen in the normal human testis: A histochemical and histoenzymatic study. J Endocrinol 43: 499-506.
15. Fawcett DW, Dym M,. 1976. A glycogen-rich segment of the tubuli recti and proximal portion of the rete testis in the guinea-pig. J Reprod Fert 38: 401-409.
16. Fouquet JP, Guha S,. 1969. Glycogen, phosphorylase and glycogen synthetase in hamster testis during postnatal development. J Reprod Fert 19: 455-464.
17. Fröjdman K, Pelliniemi LJ, Lendahl U, Virtanen I, Eriksson JE,. 1997. The intermediate filament protein nestin occurs transiently in differentiating testis of rat and mouse. Differentiation 61 (4): 243-249. (Pubitemid 27466461)
18. Gentry MS, Worby CA, Dixon JE,. 2005. Insights into Lafora disease: Malin is an E3 ubiquitin ligase that ubiquitinates and promotes the degradation of laforin. PNAS 102 (24): 8501-8506. (Pubitemid 40862765)
19. Gentry MS, Romá-Mateo C, Sanz P,. 2012. Laforin, a protein with many faces: Glucan phosphatase, adapter protein, et alii. FEBS J 280 (2): 525-537.
20. Graham TE, Yuan Z, Hill AK, Wilson RJ,. 2010. The regulation of muscle glycogen: The granule and its proteins. Acta physiol 199: 489-498.
21. Greenberg CC, Meredith KN, Yan L, Brady MJ,. 2003. Protein targeting to glycogen overexpression results in the specific enhancement of glycogen storage in 3T3-L1 adipocytes. J Biol Chem 278 (33): 30835-30842. (Pubitemid 36994592)
22. Greenberg CC, Danos AM, Brady MJ,. 2006. Central role for protein targeting to glycogen in the maintenance of cellular glycogen stores in 3T3-L1 adipocytes. Mol Cel Biol 26 (1): 334-342.
23. Hutchison GR, Scott HM, Walker M, McKinnell C, Ferrada D, Mahood IK, Sharpe RM,. 2008. Sertoli cell development and function in an animal model of testicular dysgenesis syndrome. Biol Reprod 78 (2): 352-360. (Pubitemid 351159991)
24. Ingebritsen TS, Foulkes JG, Cohen P,. 1983. The protein phosphatases involved in cellular regulation: Glycogen metabolism. Eur J Biochem 132: 263-274. (Pubitemid 13093423)
25. Kuijpers TW, Maianski NA, Tool ATJ, Smit GPA, Rake JP, Roos D, Visser G,. 2003. Apoptotic neutrophils in the circulation of patients with glycogen storage disease type 1b (GSD1b). Blood 101: 5021-5024. (Pubitemid 36857768)
26. Kuramori C, Hase Y, Hoshikawa K, Watanabe K, Nishi T, Hishiki T, Soga T, Nashimoto A, Kabe Y, Yamaguchi Y, Watanabe H, Kataoka K, Suematsu M, Handa H,. 2009. Mono-(2-ethylhexyl) phthalate targets glycogen debranching enzyme and affects glycogen metabolism in rat testis. Toxicol Sci 109 (1): 143-151.
27. Laemmli UK,. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
28. Lee W-NP, Guo P, Lim S, Bassilian S, Lee ST, Boren J, Cascante M, Go VLW, Boros LG,. 2004. Metabolic sensitivity of pancreatic tumour cell apoptosis to glycogen phosphorylase inhibitor treatment. Br J Cancer 91: 2094-2100. (Pubitemid 40128777)
29. Lobo MV, Arenas MI, Alonso FJ, Gomez G, Bazán E, Paíno CL, Fernández E, Fraile B, Paniagua R, Moyano A, Caso E,. 2004. Nestin, a neuroectodermal stem cell marker molecule is expressed in Leydig cells of the human testis and in some specific cell types from human testicular tumours. Cell Tissue Res 316 (3): 369-376. (Pubitemid 38824003)
30. Mruk DD, Cheng CY,. 2010. Tight junctions in the testis: New perspectives. Phil Trans R Soc B 365: 1621-1635.
31. Mruk DD, Cheng CY,. 2011. Desmosomes in the testis: Moving into an unchartered territory. Spermatogenesis 1 (1): 47-51.
32. Mruk DD, Yan Cheng, C,. 2004. Sertoli-sertoli and sertoli-germ cell interactions and their significance in germ cell movement in the seminiferous epithelium during spermatogenesis. Endocrine Rev 25 (5): 747-806. (Pubitemid 39362296)
33. Nakanishi Y, Shiratsuchi A,. 2004. Phagocytic removal of apoptotic spermatogenic cells by sertoli cells: Mechanism and consequences. Biol Pharm Bull 27 (1): 13-16. (Pubitemid 41656665)
34. Nuttal FQ, Gannon MC, Bai G, Lee EY,. 1994. Primary structure of human liver glycogen synthase deduced by cDNA cloning. Arch Biochem Biophys 311: 443-449. (Pubitemid 24220167)
35. Öz G, Seaquist ER, Kumar A, Criego AB, Benedict LE, Rao JP, Henry P-G, Van De Moortele P-F, Gruetter R,. 2007. Human brain glycogen content and metabolism: Implications on its role in brain energy metabolism. Am J Physiol Endocrinol Metab 292: E946-E951. (Pubitemid 46411076)
36. Preiss J, Walsh D. A,. 1981. The comparative biochemistry of glycogen and starch. In:, Ginsburg V, Robbins P, editors. Biology of carbohydrates. New York: John Wiley and Sons. pp 199-314.
37. Roach PJ,. 2011. Are there errors in glycogen biosynthesis and is laforin a repair enzyme ? FEBS Lett 585 (20): 3216-3218.
38. Roach PJ, DePaoli-Roach AA, Hurley TD, Tagliabracci S,. 2012. Glycogen and its metabolism: Some new developments and old themes. Biochem J 441: 763-787.
39. Shaha C, Tripathi R, Mishra DP,. 2010. Male germ cell apoptosis: Regulation and biology. Philos Trans R Soc Lond B Biol Sci 365 (1546): 1501-1515.
40. Solaz-Fuster MC, Gimeno-Alcañiz JV, Ros S, Fernández- Sánchez ME, García-Fojeda B, Criado-García O, Vilchez D, Dominguez J, García-Rocha M, Sánchez-Piris M, Aguado C, Knecht E, Serratosa J, Guinovart JJ, Sanz P, Rodriguez de Cõrdoba S,. 2008. Regulation of glycogen synthesis by the laforin-malin complex is modulated by the AMP-activated protein kinase pathway. Hum Mol Genet 17: 667-678. (Pubitemid 351292256)
41. Stalmans W, Bollen M, Muumbi L,. 1987. Control glycogen synthesis in health and disease. Diabetes Metab Rev 3: 127-161. (Pubitemid 17002811)
42. Stapleton D, Nelson Ch, Parsawar K, McClain D, Gilbert-Wilson R, Barker E, Rudd B, Brown K, Hendrix W, O'Donnell P, Parker G,. 2010. Analysis of hepatic glycogen-associated proteins. Proteomics 10 (12): 2320-2329.
43. Tagliabriacci VS, Heiss C, Karthik Ch, Contreras CJ, Glushka J, Ishihara M, Azadi P, Hurley TD, DePaoli-Roach AA, Roach PJ,. 2011. Phosphate incorporation during glycogen synthesis and Lafora disease. Cell Metab 13 (3): 274-282.
44. Thakur SC, Thakur SS, Chaube SK, Singh SP,. 2003. Subchronic supplementation of lithium carbonate Induces reproductive system toxicity in male rat. Reproductive Toxicol 17: 683-690. (Pubitemid 37462405)
45. Vallés-Ortega J, Durán J, García-Rocha M, Bosch C, Saez I, Pujadas Ll, Serafín A, Cañas X, Soriano E, Delgado-García JM, Gruart A, Guinovart JJ,. 2011. Neurodegeneration and functional impairments associated with glycogen synthase accumulation in a mouse model of Lafora disease. EMBO Mol Med 3: 1-15.
46. Vilchez D, Ros S, Cifuentes D, Pujadas Ll, Vallès J, García-Fojeda B, Criado-García O, Fernández-Sánchez E, Medraño-Fernández I, Domínguez J, García-Rocha M, Soriano E, Rodríguez de Cõrdoba S, Guinovart JJ,. 2007. Mechanism suppressing glycogen synthesis in neurons and its demise in progressive myoclonus epilepsy. Nat Neurosci 10 (11): 1407-1413. (Pubitemid 350014686)
47. Wender R, Brown AM, Fern R, Swanson RA, Farrell K, Ransom BR,. 2000. Astrocytic glycogen influences axon function and survival during glucose deprivation in central white matter. J Neurosci 20: 6804-6810.
48. Worby CA, Gentry MS, Dixon JE,. 2008. Malin decreases glycogen accumulation by promoting the degradation of protein targeting to glycogen (PTG). J Biol Chem 283 (7): 4069-4076.
49. Yazama F, Esaki M, Sawada H,. 1997. Immunocytochemistry of extracellular matrix components in the rat seminiferous tubules: Electron microscopic localization with improved methodology. Anat Rec 248: 51-62. (Pubitemid 27188378)
50. Zerban H, Radig S, Kopp-Schneider A, Bannasch P,. 1994. Cell proliferation and cell death (apoptosis) in hepatic preneoplasia and neoplasia are closely related to phenotypic cellular diversity and instability. Carcinogenesis 15 (11): 2467-2473. (Pubitemid 24343677)