GLP-1 Receptor Agonist Exenatide Attenuates the Detrimental Effects of Obesity on Inflammatory Profile in Testis and Sperm Quality in Mice

American Journal of Reproductive Immunology

Volumn 74, Issue 5, 2015, Pages 457-466

  Zhang, Erhong ^a   Xu, Fen ^a   Liang, Hua ^a   Yan, Jinhua ^a   Xu, Haixia ^a   Li, Zhuo ^a   Wen, Xingqiao ^a   Weng, Jianping ^a  

^a THE THIRD AFFILIATED HOSPITAL OF SUN YAT SEN UNIVERSITY   (China)

Author keywords

Fertility; GLP 1; Inflammation; Obesity; Sperm quality

Indexed keywords

EXENDIN 4; MONOCYTE CHEMOTACTIC PROTEIN 1; TESTOSTERONE; TUMOR NECROSIS FACTOR ALPHA; CYTOKINE; GLUCAGON LIKE PEPTIDE 1 RECEPTOR; INCRETIN; PEPTIDE; VENOM;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; FOOD INTAKE; HISTOPATHOLOGY; LIPID DIET; MALE; MOUSE; NONHUMAN; OBESITY; ORCHITIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SEMINAL VESICLE; SIGNAL TRANSDUCTION; SPERM QUALITY; SPERMATOZOON COUNT; SPERMATOZOON MOTILITY; TESTIS; TESTOSTERONE BLOOD LEVEL; AGONISTS; ANIMAL; DRUG EFFECTS; INFLAMMATION; METABOLISM; SPERMATOZOON;

ANIMALS; CYTOKINES; DIET, HIGH-FAT; GLUCAGON-LIKE PEPTIDE-1 RECEPTOR; INCRETINS; INFLAMMATION; MALE; MICE; OBESITY; PEPTIDES; SPERMATOZOA; TESTIS; VENOMS;

EID: 84944166687     PISSN: 10467408     EISSN: 16000897     Source Type: Journal    
DOI: 10.1111/aji.12420     Document Type: Article

References (46)

1. Flegal KM, Carroll MD, Kit BK, Ogden CL: Prevalence of obesity and trends in the distribution of body mass index among US adults, 1999-2010. JAMA 2012; 307:491-497.
2. Jensen TK, Andersson AM, Jorgensen N, Andersen AG, Carlsen E, Petersen JH, Skakkebaek NE: Body mass index in relation to semen quality and reproductive hormones among 1, 558 Danish men. Fertil Steril 2004; 82:863-870.
3. Bakos HW, Henshaw RC, Mitchell M, Lane M: Paternal body mass index is associated with decreased blastocyst development and reduced live birth rates following assisted reproductive technology. Fertil Steril 2011; 95:1700-1704.
4. McPherson NO, Fullston T, Bakos HW, Setchell BP, Lane M: Obese father's metabolic state, adiposity, and reproductive capacity indicate son's reproductive health. Fertil Steril 2014; 101:865-873.
5. Bakos HW, Mitchell M, Setchell BP, Lane M: The effect of paternal diet-induced obesity on sperm function and fertilization in a mouse model. Int J Androl 2011; 34:402-410.
6. Samavat J, Natali I, Degl'Innocenti S, Filimberti E, Cantini G, Di Franco A, Danza G, Seghieri G, Lucchese M, Baldi E, Forti G, Luconi M: Acrosome reaction is impaired in spermatozoa of obese men: a preliminary study. Fertil Steril 2014; 102:1274-1281.
7. Keltz J, Zapantis A, Jindal SK, Lieman HJ, Santoro N, Polotsky AJ: Overweight men: clinical pregnancy after ART is decreased in IVF but not in ICSI cycles. J Assist Reprod Genet 2010; 27:539-544.
8. Kriegel TM, Heidenreich F, Kettner K, Pursche T, Hoflack B, Grunewald S, Poenicke K, Glander HJ, Paasch U: Identification of diabetes- and obesity-associated proteomic changes in human spermatozoa by difference gel electrophoresis. Reprod Biomed Online 2009; 19:660-670.
9. Palmer NO, Fullston T, Mitchell M, Setchell BP, Lane M: SIRT6 in mouse spermatogenesis is modulated by diet-induced obesity. Reprod Fertil Dev 2011; 23:929-939.
10. Binder NK, Mitchell M, Gardner DK: Parental diet-induced obesity leads to retarded early mouse embryo development and altered carbohydrate utilisation by the blastocyst. Reprod Fertil Dev 2012; 24:804-812.
11. Bray GA: Medical treatment of obesity: the past, the present and the future. Best Pract Res Clin Gastroenterol 2014; 28:665-684.
12. Hakonsen LB, Thulstrup AM, Aggerholm AS, Olsen J, Bonde JP, Andersen CY, Bungum M, Ernst EH, Hansen ML, Ernst EH, Ramlau-Hansen CH: Does weight loss improve semen quality and reproductive hormones? Results from a cohort of severely obese men. Reprod Health 2011; 8:24.
13. Palmer NO, Bakos HW, Owens JA, Setchell BP, Lane M: Diet and exercise in an obese mouse fed a high-fat diet improve metabolic health and reverse perturbed sperm function. Am J Physiol Endocrinol Metab 2012; 302:E768-E780.
14. Schoeller EL, Albanna G, Frolova AI, Moley KH: Insulin rescues impaired spermatogenesis via the hypothalamic-pituitary-gonadal axis in Akita diabetic mice and restores male fertility. Diabetes 2012; 61:1869-1878.
15. Fang X, Xu QY, Jia C: Peng YF [Metformin improves epididymal sperm quality and antioxidant function of the testis in diet-induced obesity rats]. Zhonghua Nan Ke Xue 2012; 18:146-149.
16. Russell S: Incretin-based therapies for type 2 diabetes mellitus: a review of direct comparisons of efficacy, safety and patient satisfaction. Int J Clin Pharm 2013; 35:159-172.
17. George RE, Joseph S: A review of newer treatment approaches for type-2 diabetes: focusing safety and efficacy of incretin based therapy. Saudi Pharm J 2014; 22:403-410.
18. Xu W, Bi Y, Sun Z, Li J, Guo L, Yang T, Wu G, Shi L, Feng Z, Qiu L, Li Q, Guo X, Luo Z, Lu J, Shan Z, Yang W, Ji Q, Yan L, Li H, Yu X, Li S, Zhou Z, Lv X, Liang Z, Lin S, Zeng L, Yan J, Ji L, Weng J: Comparison of the effects on glycaemic control and beta-cell function in newly diagnosed type 2 diabetes patients of treatment with exenatide, insulin or pioglitazone: a multicentre randomized parallel-group trial (the CONFIDENCE study). J Intern Med 2015; 277:137-150.
19. Jensen EP, Poulsen SS, Kissow H, Holstein-Rathlou NH, Deacon CF, Jensen BL, Holst JJ, Sorensen CM: Activation of GLP-1 receptors on vascular smooth muscle cells reduces the autoregulatory response in afferent arterioles and increases renal blood flow. Am J Physiol Renal Physiol 2015; 308:F867-F877.
20. Pujante AP, Hellin GM, Roman LM, Ferrer GM, Garcia ZM, Tebar MJ: Metabolic control and weight loss in patients with obesity and type 2 diabetes mellitus, treated with exenatide. Med Clin (Barc) 2012; 139:572-578.
21. World Health Organization: WHO Laboratory Manual for the Examination and Processing of Human Semen, 5th edn. [M]. Geneva, WHO Press, 2010; 21-101.
22. Koppers AJ, Garg ML, Aitken RJ: Stimulation of mitochondrial reactive oxygen species production by unesterified, unsaturated fatty acids in defective human spermatozoa. Free Radic Biol Med 2010; 48:112-119.
23. Muriel L, Garrido N, Fernandez JL, Remohi J, Pellicer A, de Los SM, Meseguer M: Value of the sperm deoxyribonucleic acid fragmentation level, as measured by the sperm chromatin dispersion test, in the outcome of in vitro fertilization and intracytoplasmic sperm injection. Fertil Steril 2006; 85:371-383.
24. Carretero MI, Lombardo D, Arraztoa CC, Giuliano SM, Gambarotta MC, Neild DM: Evaluation of DNA fragmentation in llama (Lama glama) sperm using the sperm chromatin dispersion test. Anim Reprod Sci 2012; 131:63-71.
25. Fernandez JL, Muriel L, Goyanes V, Segrelles E, Gosalvez J, Enciso M, LaFromboise M, De Jonge C: Simple determination of human sperm DNA fragmentation with an improved sperm chromatin dispersion test. Fertil Steril 2005; 84:833-842.
26. Xu F, Li Z, Zheng X, Liu H, Liang H, Xu H, Chen Z, Zeng K, Weng J: SIRT1 mediates the effect of GLP-1 receptor agonist exenatide on ameliorating hepatic steatosis. Diabetes 2014; 63:3637-3646.
27. La Vignera S, Condorelli RA, Vicari E, Tumino D, Morgia G, Favilla V, Cimino S, Calogero AE: Markers of semen inflammation: supplementary semen analysis? J Reprod Immunol 2013; 100:2-10.
28. Winnall WR, Hedger MP: Phenotypic and functional heterogeneity of the testicular macrophage population: a new regulatory model. J Reprod Immunol 2013; 97:147-158.
29. MacDonald AA, Herbison GP, Showell M, Farquhar CM: The impact of body mass index on semen parameters and reproductive hormones in human males: a systematic review with meta-analysis. Hum Reprod Update 2010; 16:293-311.
30. Ghanayem BI, Bai R, Kissling GE, Travlos G, Hoffler U: Diet-induced obesity in male mice is associated with reduced fertility and potentiation of acrylamide-induced reproductive toxicity. Biol Reprod 2010; 82:96-104.
31. Pasquali R: Obesity and androgens: facts and perspectives. Fertil Steril 2006; 85:1319-1340.
32. Finkelstein JS, Lee H, Burnett-Bowie SA, Pallais JC, Yu EW, Borges LF, Jones BF, Barry CV, Wulczyn KE, Thomas BJ, Leder BZ: Gonadal steroids and body composition, strength, and sexual function in men. N Engl J Med 2013; 369:1011-1022.
33. Khoo J, Piantadosi C, Worthley S, Wittert GA: Effects of a low-energy diet on sexual function and lower urinary tract symptoms in obese men. Int J Obes (Lond) 2010; 34:1396-1403.
34. Jeibmann A, Zahedi S, Simoni M, Nieschlag E, Byrne MM: Glucagon-like peptide-1 reduces the pulsatile component of testosterone secretion in healthy males. Eur J Clin Invest 2005; 35:565-572.
35. Stewart TM, Liu DY, Garrett C, Jorgensen N, Brown EH, Baker HW: Associations between andrological measures, hormones and semen quality in fertile Australian men: inverse relationship between obesity and sperm output. Hum Reprod 2009; 24:1561-1568.
36. Hammoud AO, Gibson M, Peterson CM, Meikle AW, Carrell DT: Impact of male obesity on infertility: a critical review of the current literature. Fertil Steril 2008; 90:897-904.
37. Dufourc EJ: Sterols and membrane dynamics. J Chem Biol 2008; 1:63-77.
38. Ruiz-Pesini E, Lapena AC, Diez C, Alvarez E, Enriquez JA, Lopez-Perez MJ: Seminal quality correlates with mitochondrial functionality. Clin Chim Acta 2000; 300:97-105.
39. Amaral A, Lourenco B, Marques M, Ramalho-Santos J: Mitochondria functionality and sperm quality. Reproduction 2013; 146:R163-R174.
40. Piomboni P, Focarelli R, Stendardi A, Ferramosca A, Zara V: The role of mitochondria in energy production for human sperm motility. Int J Androl 2012; 35:109-124.
41. Song SH, Lim JJ, Bang JK, Cha SK, Lee DR, Kim YS, Ahn TY, Yoon TK: Evaluation of sperm deoxyribonucleic acid (DNA) damage and effects on embryo development using a mouse cryptorchidism model. Urology 2013; 82:717-743.
42. Belloc S, Benkhalifa M, Cohen-Bacrie M, Dalleac A, Chahine H, Amar E, Zini A: Which isolated sperm abnormality is most related to sperm DNA damage in men presenting for infertility evaluation. J Assist Reprod Genet 2014; 31:527-532.
43. Schulte RT, Ohl DA, Sigman M, Smith GD: Sperm DNA damage in male infertility: etiologies, assays, and outcomes. J Assist Reprod Genet 2010; 27:3-12.
44. Dupont C, Faure C, Sermondade N, Boubaya M, Eustache F, Clement P, Briot P, Berthaut I, Levy V, Cedrin-Durnerin I, Benzacken B, Chavatte-Palmer P, Levy R: Obesity leads to higher risk of sperm DNA damage in infertile patients. Asian J Androl 2013; 15:622-625.
45. Perdichizzi A, Nicoletti F, La Vignera S, Barone N, D'Agata R, Vicari E, Calogero AE: Effects of tumour necrosis factor-alpha on human sperm motility and apoptosis. J Clin Immunol 2007; 27:152-162.
46. Fraczek M, Szumala-Kakol A, Dworacki G, Sanocka D, Kurpisz M: In vitro reconstruction of inflammatory reaction in human semen: effect on sperm DNA fragmentation. J Reprod Immunol 2013; 100:76-85.