Metabolic profile changes in the testes of mice with streptozotocin-induced type 1 diabetes mellitus

International Journal of Andrology

Volumn 32, Issue 2, 2009, Pages 156-165

  Mallidis, C ^a,b   Green, B D ^b   Rogers, D ^a   Agbaje, I M ^a   Hollis, J ^b   Migaud, M ^b   Amigues, E ^b   McClure, N ^a   Browne, R A ^b  

^a QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

^b QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

Author keywords

Diabetes; Metabolites; Spermatogenesis; Testis

Indexed keywords

ALANINE; BETAINE; CARNITINE; CHOLINE; CREATINE; GLUCOSE; HEMOGLOBIN A1C; INOSITOL; LACTIC ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; C57BL 6 MOUSE; CONTROLLED STUDY; GLUCOSE BLOOD LEVEL; MALE; MALE GENITAL SYSTEM FUNCTION; METABOLOMICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; STREPTOZOCIN DIABETES; TESTIS; WEIGHT REDUCTION; ANIMAL; C57BL MOUSE; EXPERIMENTAL DIABETES MELLITUS; FERTILITY; INSULIN DEPENDENT DIABETES MELLITUS; METABOLISM; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PATHOPHYSIOLOGY; PRINCIPAL COMPONENT ANALYSIS; SPERMATOGENESIS;

ANIMALS; BETAINE; CARNITINE; CHOLINE; CREATINE; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 1; FERTILITY; MAGNETIC RESONANCE SPECTROSCOPY; MALE; MICE; MICE, INBRED C57BL; PRINCIPAL COMPONENT ANALYSIS; SPERMATOGENESIS; TESTIS;

EID: 61849123187     PISSN: 01056263     EISSN: 13652605     Source Type: Journal    
DOI: 10.1111/j.1365-2605.2007.00829.x     Document Type: Article

References (50)

1. Abdel-Aziz, M. T., Abdel-Kader, M. M. Rashad, M. M. (1975) Urinary catecholamines and their metabolites in diabetes. Acta Biologica et Medica Germanica 34, 710, 1643 1650.
2. Agbaje, I. M., Rogers, D. A., McVicar, C. M., McClure, N., Atkinson, A. B., Mallidis, C. Lewis, S. E. M. (2007) Insulin dependant diabetes mellitus: implications for male reproductive function. Human Reproduction 22, 1871 1877.
3. Ali, S. T., Shaikh, R. N., Siddiqi, N. A. Siddiqi, P. Q. (1993) Semen analysis in insulin-dependent/non-insulin-dependent diabetic men with/without neuropathy. Archives of Andrology 30, 47 54.
4. Amaral, S., Moreno, A. J., Santos, M. S., Seica, R. Ramalho-Santos, J. (2006) Effects of hyperglycemia on sperm and testicular cells of Goto-Kakizaki and streptozotocin-treated rat models for diabetes. Theriogenology 66, 2056 2067.
5. Babbott, D., Rubin, A. Ginsburg, S. J. (1958) The reproductive characteristics of diabetic men. Diabetes 7, 33 35.
6. Bjorgaas, M., Vik, T., Sager, G., Sagen, E. Jorde, R. (1997) Urinary excretion of adrenaline and noradrenaline during hypoglycaemic clamp in diabetic and non-diabetic adolescents. Scandinavian Journal of Clinical and Laboratory Investigation 57, 711 718.
7. Boussouar, F. Benahmed, M. (2004) Lactate and energy metabolism in male germ cells. Trends in Endocrinology and Metabolism, 15 345 350.
8. Bray, C., Son, J. H. Meizel, S. (2005) Acetylcholine causes an increase of intracellular calcium in human sperm. Molecular Human Reproduction 11, 881 889.
9. Brindle, J. T., Antti, H., Holmes, E., Tranter, G., Nicholson, J. K., Bethell, H. W. et al. (2002) Rapid and noninvasive diagnosis of the presence and severity of coronary heart disease using 1H-NMR-based metabonomics. Nature Medicine 8, 1439 1444.
10. Connor, S. C., Wu, W., Sweatman, B. C., Manini, J., Haselden, J. N., Crowther, D. J. Waterfield, C. J (2006) Effects of feeding and body weight loss on the 1H-NMR-based urine metabolic profiles of male Wistar Han rat: implications for biomarker discovery. Biomarkers 9, 156 179.
11. Deana, R., Rigoni, F., Francesconi, M., Cavallini, L., Arslan, P. Siliprandi, N. (1989) Effect of L-carnitine and L-aminocarnitine on calcium transport, motility, and enzyme release from ejaculated bovine spermatozoa. Biology of Reproduction 41, 949 955.
12. Dellow, W. J., Chambers, S. T., Lever, M., Lunt, H. Robson, R. A. (1999) Elevated glycine betaine excretion in diabetes mellitus patients is associated with proximal tubular dysfunction and hyperglycemia. Diabetes Research and Clinical Practice 43, 91 99.
13. Dellow, W. J., Chambers, S. T., Barrell, G. K., Lever, M. Robson, R. A. (2001) Glycine betaine excretion is not directly linked to plasma glucose concentrations in hyperglycaemia. Diabetes Research and Clinical Practice 52, 165 169.
14. Draper, R. P. Timbrell, J. A. (1996) Urinary creatine as a potential marker of testicular damage: effect of vasectomy. Reproductive Toxicology 10, 79 85.
15. Dunne, V. G., Bhattachayya, S., Besser, M., Rae, C. Griffin, J. L. (2005) Metabolites from cerebrospinal fluid in aneurysmal subarachnoid haemorrhage correlate with vasospasm and clinical outcome: a pattern-recognition 1H NMR study. NMR in Biomedicine 18, 24 33.
16. Enomoto, A., Wempe, M. F., Tsuchida, H., Shin, H. J., Cha, S. H., Anzai, N. et al. (2002) Molecular identification of a novel carnitine transporter specific to human testis. Insights into the mechanism of carnitine recognition. Journal of Biological Chemistry 277, 36262 36271.
17. Fan, T. W. M. (1996) Metabolite profiling by one- and two-dimensional NMR analysis of complex mixtures. Progress in Nuclear Magnetic Spin Resonance 28, 161 219.
18. Frenkel, G. P., Homonnai, Z. T., Drasnin, N., Sofer, A., Kaplan, R. Kraicer, P. F. (1978) Fertility of the streptozotocin-diabetic male rat. Andrologia 10, 127 136.
19. Griffin, J. L., Troke, J., Walker, L. A., Shore, R. F., Lindon, J. C. Nicholson, J. K. (2000) The biochemical profile of rat testicular tissue as measured by magic angle spinning 1H NMR spectroscopy. FEBS Letters 486, 225 229.
20. Hamamah, S., Seguin, F., Bujan, L., Barthelemy, C., Mieusset, R. Lansac, J. (1998) Quantification by magnetic resonance spectroscopy of metabolites in seminal plasma able to differentiate different forms of azoospermia. Human Reproduction 13, 132 135.
21. Hamilton, B. E. Ventura, S. J. (2006) Fertility and abortion rates in the United States, 1960-2002. International Journal of Andrology 29, 34 45.
22. Handelsman, D. J., Conway, A. J., Boylan, L. M., Yue, D. K. Turtle, J. R. (1985) Testicular function and glycemic control in diabetic men. A controlled study. Andrologia 17, 488 496.
23. Hinton, B. T. Setchell, B. P. (1980) Concentrations of glycerophosphocholine, phosphocholine and free inorganic phosphate in the luminal fluid of the rat testis and epididymis. Journal of Reproduction and Fertility 58, 401 406.
24. Holmes, E., Tsang, T. M., Huang, J. T., Leweke, F. M., Koethe, D., Gerth, C. W. et al. (2006) Metabolic profiling of CSF: evidence that early intervention may impact on disease progression and outcome in schizophrenia. PLoS Medicine 3, 1420 1427.
25. Jensen, T. K., Carlsen, E., Jorgensen, N., Berthelsen, J. G., Keiding, N., Christensen, K., Petersen, J. H., Knudsen, L. B. Skakkebaek, N. E. (2002) Poor semen quality may contribute to recent decline in fertility rates. Human Reproduction, 17, 1437 1440.
26. Kalter-Leibovici, O., Wainstein, J., Ziv, A., Harman-Bohem, I., Murad, H., Raz, I. Israel Diabetes Research Group (IDRG) Investigators (2005) Clinical, socioeconomic, and lifestyle parameters associated with erectile dysfunction among diabetic men. Diabetes Care 28, 1739 1744.
27. Kelly, T. L., Neaga, O. R., Schwahn, B. C., Rozen, R. Trasler, J. M. (2005) Infertility in 5,10-methylenetetrahydrofolate reductase (MTHFR)-deficient male mice is partially alleviated by lifetime dietary betaine supplementation. Biology of Reproduction 72, 667 677.
28. Kokk, K., Verajankorva, E., Wu, X.K., Tapfer, H., Poldoja, E. Pollanen, P. (2004) Immunohistochemical detection of glucose transporters class I subfamily in the mouse, rat and human testis. Medicina (Kaunas) 40, 156 160.
29. de Kretser, D. M. (1996) Declining sperm counts. BMJ 312 457 458.
30. Lawler, J. M., Barnes, W. S., Wu, G., Song, W. Demaree, S. (2002) Direct antioxidant properties of creatine. Biochemical and Biophysical Research Communications 290, 47 52.
31. Lee, H., Kim, J. H., Chae, Y. J., Ogawa, H., Lee, M. H. Gerton, G. L. (1998) Creatine synthesis and transport systems in the male rat reproductive tract. Biology of Reproduction 58, 1437 1444.
32. Lewis, S. E. Aitken, R. J. (2005) DNA damage to spermatozoa has impacts on fertilization and pregnancy. Cell and Tissue Research 322, 33 41.
33. Mallidis, C., Agbaje, I., Rogers, D., Glenn, J., McCullough, S., Atkinson, A. B., Steger, K., Stitt, A. McClure, N. (2007) Distribution of the receptor for advanced glycation end products in the human male reproductive tract: prevalence in men with diabetes mellitus. Human Reproduction 22, 2169 2177.
34. Morgan, S. P. (2003) Is low fertility a twenty-first-century demographic crisis Demography 40, 589 603.
35. Morris, I. D., Ilott, S., Dixon, L. Brison, D. R. (2002) The spectrum of DNA damage in human sperm assessed by single cell gel electrophoresis (Comet assay) and its relationship to fertilization and embryo development. Human Reproduction 17, 990 998.
36. Ng, C. M., Blackman, M. R., Wang, C. Swerdloff, R. S. (2004) The role of carnitine in the male reproductive system. Annals of the New York Academy of Sciences 1033, 177 188.
37. Niven, M. J., Hitman, G. A. Badenoch, D. F. (1995) A study of spermatozoal motility in type 1 diabetes mellitus. Diabetic Medicine 12, 921 924.
38. Noppinger, K., Morrison, R., Jones, N. H. Hopkins, H. II. (1987) An evaluation of an enzymatic choline determination for the identification of semen in casework samples. Journal of Forensic Sciences 32, 1069 1074.
39. Pignatelli, P., Lenti, L., Sanguigni, V., Frati, G., Simeoni, I., Gazzaniga, P. P., Pulcinelli, F. M. Violi, F. (2003) Carnitine inhibits arachidonic acid turnover, platelet function, and oxidative stress. American Journal of Physiology 284, H41 H48.
40. Rancour, T. P. Wells, W. W. (1980) Myo-inositol metabolism in rat testis in response to streptozotocin-induced diabetes. Archives of Biochemistry and Biophysics 202, 150 159.
41. Robinson, R. Fritz, I. B. (1979) Myoinositol biosynthesis by Sertoli cells, and levels of myoinositol biosynthetic enzymes in testis and epididymis. Canadian Journal of Biochemistry 57, 962 967.
42. Sachan, D. S., Hongu, N. Johnsen, M. (2005) Decreasing oxidative stress with choline and carnitine in women. Journal of the American College of Nutrition 24, 172 176.
43. Santoro, A., Lioi, M. B., Monfregola, J., Salzano, S., Barbieri, R. Ursini, M. V. (2005) L-Carnitine protects mammalian cells from chromosome aberrations but not from inhibition of cell proliferation induced by hydrogen peroxide. Mutation Research 587, 16 25.
44. Sastry, B. V. Sadavongvivad, C. (1978) Cholinergic systems in non-nervous tissues. Pharmacological Reviews 30, 65 132.
45. Sharaf, A. A., el-Din, A. K., Hamdy, M. A. Hafeiz, A. A. (1978) Effect of ascorbic acid on oxygen consumption, glycolysis and lipid metabolism of diabetic rat testis. Ascorbic acid and diabetes, I. Journal of Clinical Chemistry and Clinical Biochemistry 16, 651 655.
46. Swamy-Mruthinti, S. Carter, A. L. (1999) Acetyl-L-carnitine decreases glycation of lens proteins: in vitro studies. Experimental Eye Research 69, 109 115.
47. Szkudelski, T. (2001) The mechanism of alloxan and streptozotocin action in B cells of the rat pancreas. Physiological Research 50, 537 546.
48. Vicari, E. Calogero, A. E. (2001) Effects of treatment with carnitines in infertile patients with prostato-vesiculo-epididymitis. Human Reproduction 16, 2338 2342.
49. Vignon, F., Le Faou, A., Montagnon, D., Pradignac, A., Cranz, C., Winiszewsky, P. Pinget, M. (1991) Comparative study of semen in diabetic and healthy men. Diabete et Metabolisme 17, 350 354.
50. Yamaguchi, M., Mitsumori, F., Watanabe, H., Takaya, N. Minami, M. (2006) In vivo localized 1H MR spectroscopy of rat testes: stimulated echo acquisition mode (STEAM) combined with short TI inversion recovery (STIR) improves the detection of metabolite signals. Magnetic Resonance in Medicine 55, 749 754.