Paternal effect on embryo quality in diabetic mice is related to poor sperm quality and associated with decreased glucose transporter expression

Reproduction

Volumn 136, Issue 3, 2008, Pages 313-322

  Kim, Sung Tae ^a   Moley, Kelle H ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3(OR 17)BETA HYDROXYSTEROID DEHYDROGENASE; GLUCOSE TRANSPORTER; GLUCOSE TRANSPORTER 1; GLUCOSE TRANSPORTER 3; GLUCOSE TRANSPORTER 5; GLUCOSE TRANSPORTER 8; GLUCOSE TRANSPORTER 9A; GLUCOSE TRANSPORTER 9B; INSULIN; STREPTOZOCIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLASTOCYST; CELL DIVISION; CONTROLLED STUDY; DEVELOPMENTAL DISORDER; EMBRYO; EMBRYO DEVELOPMENT; FERTILIZATION; FERTILIZATION IN VITRO; IMMUNOFLUORESCENCE TEST; INSULIN DEPENDENT DIABETES MELLITUS; LEYDIG CELL; MALE; MALE INFERTILITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SEMEN ANALYSIS; SPERMATOGENESIS; SPERMATOZOON ABNORMALITY; SPERMATOZOON CAPACITATION; SPERMATOZOON DENSITY; SPERMATOZOON MOTILITY; STREPTOZOCIN DIABETES; SUBFERTILITY; TESTIS; WESTERN BLOTTING; ZYGOTE;

ANIMALS; BLOTTING, WESTERN; CELLS, CULTURED; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 1; EMBRYONIC DEVELOPMENT; FEMALE; FERTILIZATION IN VITRO; FLUORESCENT ANTIBODY TECHNIQUE; GLUCOSE TRANSPORT PROTEINS, FACILITATIVE; INFERTILITY, MALE; INSULIN; LEYDIG CELLS; MALE; MICE; MICE, INBRED STRAINS; MICE, MUTANT STRAINS; MODELS, ANIMAL; SPERM COUNT; SPERM MOTILITY; SPERMATOZOA; TESTIS;

MUS;

EID: 53749089440     PISSN: 14701626     EISSN: None     Source Type: Journal    
DOI: 10.1530/REP-08-0167     Document Type: Article

References (57)

1. Aitken RJ, Clarkson LS & Fishel S 1989 Generation of reactive oxygen species, lipid peroxidation, and human sperm function. Biology of Reproduction 41 183-197.
2. Amann RP, Hammerstedt RH & Veeramachaneni DN 1993 The epididymis and sperm maturation: A perspective. Reproduction, Fertility, and Development 5 361-381.
3. Aquila S, Gentile M, Middea E, Catalano S & Ando S 2005 Autocrine regulation of insulin secretion in human ejaculated spermatozoa. Endocrinology 146 552-557.
4. Baccetti B, La Marca A, Piomboni P, Capitani S, Bruni E, Petraglia F & De Leo V 2002 Insulin-dependent diabetes in men is associated with hypothalamo-pituitary derangement and with impairment in semen quality. Human Reproduction 17 2673-2677.
5. Barber AJ, Antonetti DA, Kern TS, Reiter CE, Soans RS, Krady JK, Levison SW, Gardner TW & Bronson SK 2005 The Ins2Akita mouse as a model of early retinal complications in diabetes. Investigative Ophthalmology & Visual Science 46 2210-2218.
6. Burant CF & Davidson NO 1994 GLUT3 glucose transporter isoform in rat testis: Localization, effect of diabetes mellitus, and comparison to human testis. American Journal of Physiology 267 R1488-R1495.
7. Carayannopoulos M, Chi M, Cui Y, Pingsterhaus J & Moley K 2000 SLC2A8, a glucose transporter responsible for insulin-stimulated uptake in the blastocyst. PNAS 97 7313-7318.
8. Carayannopoulos MO, Schlein A, Wyman A, Chi M, Keembiyehetty C & Moley KH 2004 SLC2A9 is differentially expressed and targeted in the preimplantation embryo. Endocrinology 145 1435-1443.
9. Chen CS, Chao HT, Pan RL & Wei YH 1997 Maintenance of human sperm motility and prevention of oxidative damage through co-culture incubation. Andrologia 29 227-233.
10. Chen Y, Nagpal ML & Lin T 2003 Expression and regulation of glucose transporter 8 in rat Leydig cells. Journal of Endocrinology 179 63-72.
11. Chi MM, Pingsterhaus J, Carayannopoulos M & Moley KH 2000a Decreased glucose transporter expression triggers BAX-dependent apoptosis in the murine blastocyst. Journal of Biological Chemistry 275 40252-40257.
12. Chi MM, Schlein AL & Moley KH 2000b High insulin-like growth factor 1 (IGF-1) and insulin concentrations trigger apoptosis in the mouse blastocyst via down-regulation of the IGF1 receptor. Endocrinology 141 4784-4792.
13. Cooper TG 1998 Interactions between epididymal secretions and spermatozoa. Journal of Reproduction and Fertility Supplement 53 119-136.
14. Das UG, Sadiq HF, Soares MJ, Hay WW Jr & Devaskar SU 1998 Time-dependent physiological regulation of rodent and ovine placental glucose transporter (GLUT-1) protein. American Journal of Physiology 274 R339-R347.
15. Doege H, Schurmann A, Bahrenberg G, Brauers A & Joost HG 2000 SLC2A8, a novel member of the sugar transport facilitator family with glucose transport activity. Journal of Biological Chemistry 275 16275-16280.
16. Eng GS, Sheridan RA, Wyman A, Chi MM-Y, Bibee KP, Jungheim ES & Moley KH 2007 AMPK activation increases glucose uptake, decreases apoptosis and improves pregnancy outcome in embryos exposed to high IGF-1 concentrations. Diabetes 57 2228-2234.
17. Freeman JE & Wolf CR 1994 Evidence against a role for serine 129 in determining murine cytochrome P450 Cyp2e-1 protein levels. Biochemistry 33 13963-13966.
18. Giron MD, Salto R, Gonzalez Y, Giron JA, Nieto N, Periago JL, Suarez MD & Hortelano P 1999 Modulation of hepatic and intestinal glutathione S-transferases and other antioxidant enzymes by dietary lipids in streptozotocin diabetic rats. Chemosphere 38 3003-3013.
19. Glenn DR, McClure N & Lewis SE 2003 The hidden impact of diabetes on male sexual dysfunction and fertility. Human Fertility 6 174-179.
20. Gomez O, Romero A, Terrado J & Mesonero JE 2006 Differential expression of glucose transporter SLC2A8 during mouse spermatogenesis. Reproduction 131 63-70.
21. Gorovits N, Cui L, Busik JV, Ranalletta M, Hauguel de-Mouzon S & Charron MJ 2003 Regulation of hepatic SLC2A8 expression in normal and diabetic models. Endocrinology 144 1703-1711.
22. Hahn T, Barth S, Weiss U, Mosgoeller W & Desoye G 1998 Sustained hyperglycemia in vitro down-regulates the GLUT1 glucose transport system of cultured human term placental trophoblast: A mechanism to protect fetal development? FASEB Journal 12 1221-1231.
23. Han XX, Handberg A, Petersen LN, Ploug T & Galbo H 1995 Stability of GLUT-1 and GLUT-4 expression in perfused rat muscle stimulated by insulin and exercise. Journal of Applied Physiology 78 46-52.
24. Ibberson M, Riederer BM, Uldry M, Guhl 8, Roth J & Thorens B 2002 Immunolocalization of GLUTX1 in the testis and to specific brain areas and vasopressin-containing neurons. Endocrinology 143 276-284.
25. Janny L & Menezo YJ 1994 Evidence for a strong paternal effect on human preimplantation embryo development and blastocyst formation. Molecular Reproduction and Development 38 36-42.
26. Joost HG & Thorens B 2001 The extended GLUT-family of sugar/ polyol transport facilitators: Nomenclature, sequence characteristics, and potential function of its novel members (review). Molecular Membrane Biology 18 247-256.
27. Joost HG, Bell GI, Best JD, Birnbaum MI, Charron MJ, Chen YT, Doege H, James DE, Lodish HF, Moley KH et al. 2002 Nomenclature of the GLUT/SLC2A family of sugar/polyol transport facilitators. American Journal of Physiology. Endocrinology and Metabolism 282 E974-E976.
28. Kao SH, Chao HT & Wei YH 1998 Multiple deletions of mitochondrial DNA are associated with the decline of motility and fertility of human spermatozoa. Molecular Human Reproduction 4 657-666.
29. Keembiyehetty C, Augustin R, Carayannopoulos MO, Steer S, Manolescu A, Cheeseman CJ & Moley KH 2006 Mouse glucose transporter 9 splice variants are expressed in adult liver and kidney and are up-regulated in diabetes. Molecular Endocrinology 20 686-697.
30. Keim AL, Chi MM & Moley KH 2001 Hyperglycemia-induced apoptotic cell death in the mouse blastocyst is dependent on expression of p53. Molecular Reproduction and Development 60 214-224.
31. Kim ST & Moley KH 2007 Glucose transporter (GLUT) 8, SLC2A9a and SLC2A9b protein expression in the mouse testis and sperm. Reproductive Sciences 14 445-455.
32. Lee PD, Giudice LC, Conover CA & Powell DR 1997 insulin-like growth factor binding protein-1: Recent findings and new directions. Proceedings of the Society for Experimental Biology and Medicine 216 319-357.
33. Menezo YJ 2006 Paternal and maternal factors in preimplantation embryogenesis: Interaction with the biochemical environment. Reproductive Biomedicine Online 12 616-621.
34. Moley KH, Chi MM-Y, Knudson CM, Korsmeyer SJ & Mueckler MM 1998a Hyperglycemia induces apoptosis in preimplantation embryos via cell death effector pathways. Nature Medicine 12 1421-1424.
35. Moley KH, Chi MM-Y & Mueckler M 1998b Maternal hyperglycemia alters glucose transport and utilization in mouse preimplantation embryos. American Journal of Physiology 275 E38-E47.
36. Murray FT, Cameron DF & Orth JM 1983 Gonadal dysfunction in the spontaneously diabetic BB rat. Metabolism 32 141-147.
37. Nakayama Y, Yamamoto T & Abe SI 1999 IGF-I, IGF-II and insulin promote differentiation of spermatogonia to primary spermatocytes in organ culture of newt testes. International Journal of Developmental Biology 43 343-347.
38. Nasr-Esfahani MH, Salehi M, Razavi S, Anjomshoa M, Rozbahani S, Moulavi F & Mardani M 2005 Effect of sperm DNA damage and sperm protannine deficiency on fertilization and embryo development post-ICSI. Reproductive Biomedicine Online 11 198-205.
39. Ohkawa K, Ohishi N & Yagi K 1979 Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Analytical Biochemistry 95 351-358.
40. Phay JE, Hussain HB & Moley JF 2000 Cloning and expression analysis of a novel member of the facilitative glucose transporter family, SLC2A9 (SLC2A9). Genomics 66 217-220.
41. Pinto A, Carayannopoulos M, Hoehn A, Dowd L & Moley K 2002 SLC2A8 expression and translocation are critical for murine blastocyst survival. Biology of Reproduction 66 1729-1733.
42. Renard JP & Babinet C 1986 Identification of a paternal developmental effect on the cytoplasm of one-cell-stage mouse embryos. PNAS 83 6883-6886.
43. Riley JK, Carayannopoulos MO, Wyman AH, Chi M & Moley KH 2006 Phosphatidylinositol 3-kinase activity is critical for glucose metabolism and embryo survival in murine blastocysts. Journal of Biological Chemistry 281 6010-6019.
44. Rossini AA, Appel MC, Williams RM & Like AA 1977 Genetic influence of the streptozotocin-induced insulitis and hyperglycemia. Diabetes 26 916-920.
45. Sakkas D, Urner F, Menezo V & Leppens G 1993 Effects of glucose and fructose on fertilization, cleavage, and viability of mouse embryos in vitro. Biology of Reproduction 49 1288-1292.
46. Sanguinetti RE, Ogawa K, Kurohmaru M & Hayashi Y 1995 Ultrastructural changes in mouse Leydig cells after streptozotocin administration. Experimental Animals 44 71-73.
47. Scarano WR, Messias AG, Oliva SU, Klinefelter GR & Kempinas WG 2006 Sexual behaviour, sperm quantity and quality after short-term streptozotocin-induced hyperglycaemia in rats. International Journal of Andrology 29 482-488.
48. Schurmann A, Axer H, Scheepers A, Doege H & Joost HG 2002 The glucose transport facilitator SLC2A8 is predominantly associated with the acrosomal region of mature spermatozoa. Cell and Tissue Research 307 237-242.
49. Seethalakshmi L, Menon M & Diamond D 1987 The effect of streptozotocin-incluced diabetes on the neuroendocrine-male reproductive tract axis of the adult rat. Journal of Urology 138 190-194.
50. Sexton WJ & Jarow JP 1997 Effect of diabetes mellitus upon male reproductive function. Urology 49 508-513.
51. Shrivastav P, Swann J, Jeremy JY, Thompson C, Shaw RW & Dandona P 1989 Sperm function and structure and seminal plasma prostanoid concentrations in men with IDDM. Diabetes Care 12 742-744.
52. Silvestroni L, Modesti A & Sartori C 1992 Insulin-sperm interaction: Effects on plasma membrane and binding to acrosome. Archives of Andrology 28 201-211.
53. Tesarik J 2005 Paternal effects on cell division in the human preimplantation embryo. Reproductive Biomedicine Online 10 370-375.
54. Urner F & Sakkas D 1996 Glucose participates in sperm-oocyte fusion in the mouse. Biology of Reproduction 55 917-922.
55. Wang J, Takeuchi T, Tanaka S, Kubo SK, Kayo T, Lu D, Takata K, Koizumi A & Izumi T 1999 A mutation in the insulin 2 gene induces diabetes with severe pancreatic beta-cell dysfunction in the Mody mouse. Journal of Clinical Investigation 103 27-37.
56. Wiemsperger NF 2003 Oxidative stress as a therapeutic target in diabetes: Revisiting the controversy. Diabetes & Metabolism 29 579-585.
57. Wood JS & Trayhum P 2003 Glucose transporters (GLUT and SGLT): expanded families of sugar transport proteins. British Journal of Nutrition 89 3-9.