Prepubertal nutrition alters Leydig cell functional capacity and timing of puberty

English version

Autoři: Ravinder Anand-Ivell ^aff001; Colin J. Byrne ^aff002; Jonas Arnecke ^aff001; Sean Fair ^aff004; Pat Lonergan ^aff003; David A. Kenny ^aff002; Richard Ivell ^aff001
Působiště autorů: School of Biosciences, University of Nottingham, Sutton Bonington, United Kingdom ^aff001; Animal and Bioscience Department, Teagasc, Dunsany, Ireland ^aff002; School of Agriculture and Food Science, University College Dublin, Dublin, Ireland ^aff003; Laboratory of Animal Reproduction, Department of Biological Sciences, University of Limerick, Limerick, Ireland ^aff004
Vyšlo v časopise: PLoS ONE 14(11)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0225465

Souhrn

Leydig cell functional capacity reflects the numbers and differentiation status of the steroidogenic Leydig cells in the testes and becomes more or less fixed in early adulthood with the final establishment of the hypothalamo-pituitary-gonadal (HPG) axis after puberty. Factors influencing Leydig cell functional capacity and its role in puberty are poorly understood. Using a bovine model of dairy bulls fed four different nutritional regimes from 1 month to 12 months, and applying circulating Insulin-like peptide 3 (INSL3) as an accurate biomarker of Leydig cell functional capacity, showed that a high plane of nutrition in the first 6 months of life, but not later, significantly increased INSL3 in young adulthood. Moreover, INSL3 concentration at 4 months indicated a marked differential in early feeding regime and correlated well (negatively) with the timing of puberty, as reflected by the age in days for the first production of an ejaculate with >50 million sperm and >10% forward motility, as well as with testis size at 18 months. Reversing the diet at 6 months was unable to rectify the trend in either parameter, unlike for other parameters such as testosterone, body weight, and scrotal circumference. This study has shown that early prepubertal nutrition is a key factor in the development of Leydig cell functional capacity in early adulthood and appears to be a key driver in the dynamic progression of puberty.

Klíčová slova:

Body weight – Cell differentiation – Puberty – Sperm – Spermatogenesis – Testes – Testosterone

Zdroje

1. Teerds KJ, Huhtaniemi IT. Morphological and functional maturation of Leydig cells: from rodent models to primates. Hum Reprod Update. 2015; 21:310–328. doi: 10.1093/humupd/dmv008 25724971

2. Ivell R, Wade JD, Anand-Ivell R. Insulin-like factor 3 (INSL3) as a biomarker of Leydig cell functional capacity. Biol Reprod. 2013; 88:147. doi: 10.1095/biolreprod.113.108969 23595905

3. Anand-Ivell RJK, Wohlgemuth J, Haren MT, Hope PJ, Hatzinikolas G, Wittert G et al. Peripheral INSL3 concentrations decline with age in a large population of Australian men. Int J Androl. 2006; 29:618–626. doi: 10.1111/j.1365-2605.2006.00714.x 17014531

4. Byrne CJ, Fair S, English AM, Cirot M, Staub C, Lonergan P et al. Plane of nutrition before and after 6 months of age in Holstein-Friesian bulls: I. Effects on performance, body composition, age at puberty, and postpubertal semen production. J Dairy Sci. 2018; 101:3447–3459. doi: 10.3168/jds.2017-13719 29428748

5. Wolf F, Almquist J, Hale E. Prepuberal behavior and puberal characteristics of beef bulls on high nutrient allowance. J Anim Sci. 1965; 24:761–765. doi: 10.2527/jas1965.243761x 14313741

6. Brito LFC, Silva AEDF, Unanian MM, Dode MAN, Barbosa RT, Kastelic JP. Sexual development in early- and late-maturing Bos indicus and Bos indicus × Bos taurus crossbred bulls in Brazil. Theriogenology. 2004; 62:1198–1217. doi: 10.1016/j.theriogenology.2004.01.006 15325547

7. Kenny DA, Heslin J, Byrne CJ. Early onset of puberty in cattle: implications for gamete quality and embryo survival. Reprod Fertil Dev. 2017; 30:101–117. doi: 10.1071/RD17376 29539307

8. Murphy EM, Kelly AK, O'Meara C, Eivers B, Lonergan P, Fair S. Influence of bull age, ejaculate number, and season of collection on semen production and sperm motility parameters in Holstein Friesian bulls in a commercial artificial insemination centre. J Anim Sci. 2018; 96:2408–2418. doi: 10.1093/jas/sky130 29767722

9. Rawlings N, Evans AC, Chandolia RK, Bagu ET. Sexual maturation in the bull. Reprod Domest Anim. 2008; 43 Suppl 2:295–301.

10. McGowan M, Holland MK, Boe-Hansen G. Ontology and endocrinology of the reproductive system of bulls from fetus to maturity. Animal. 2018; 12:s19–s26. doi: 10.1017/S1751731118000460 29551096

11. Plant TM. The hypothalamo-pituitary-gonadal axis. J Endocrinol. 2015; 226:T41–54. doi: 10.1530/JOE-15-0113 25901041

12. Ivell R, Spiess A. Analysing differential gene expression in the testis. Ernst Schering Research Foundation Workshop, Suppl 9 ‘Testicular Tangrams’ (ed. Rommerts FFG & Teerds KJ), 2002; pp99-120.

13. Ivell R, Anand-Ivell R. The biology of Insulin-like Factor 3 (INSL3) in human reproduction. Hum Reprod Update. 2009; 15:463–476. doi: 10.1093/humupd/dmp011 19329805

14. Chong YH, Pankhurst MW, McLennan IS. The daily profiles of circulating AMH and INSL3 in men are distinct from the other testicular hormones, inhibin B and testosterone. PLoS One. 2015; 10:e0133637. doi: 10.1371/journal.pone.0133637 26192622

15. Sadeghian H, Anand-Ivell R, Balvers M, Relan V, Ivell R. Constitutive regulation of the Insl3 gene in rat Leydig cells. Mol Cell Endocrinol. 2005; 241:10–20. doi: 10.1016/j.mce.2005.03.017 16006031

16. Anand-Ivell R, Heng K, Hafen B, Setchell B, Ivell R. Dynamics of INSL3 peptide expression in the rodent testis. Biol Reprod. 2009; 81:480–487. doi: 10.1095/biolreprod.109.077552 19420383

17. Ivell R, Agoulnik AI, Anand-Ivell R. Relaxin-like peptides in male reproduction—a human perspective. Br J Pharmacol. 2017; 174:990–1001. doi: 10.1111/bph.13689 27933606

18. Hannan MA, Fukami Y, Kawate N, Sakase M, Fukushima M, Pathirana IN et al. Plasma insulin-like peptide 3 concentrations are acutely regulated by luteinizing hormone in pubertal Japanese Black beef bulls. Theriogenology. 2015; 84:1530–1535. doi: 10.1016/j.theriogenology.2015.07.039 26318230

19. Ivell R, Heng K, Anand-Ivell R. Insulin-like factor 3 (INSL3) and the HPG axis in the male. Front Endocrinol. 2014; 5:6.

20. Bathgate R, Balvers M, Hunt N, Ivell R. The relaxin like factor (RLF) is upregulated in the bovine ovary of the cycle and pregnancy: sequence and mRNA analysis. Biol Reprod. 1996; 55:1452–1457. doi: 10.1095/biolreprod55.6.1452 8949906

21. Kawate N, Ohnari A, Pathirana IN, Sakase M, Büllesbach EE, Takahashi M et al. Changes in plasma concentrations of insulin-like peptide 3 and testosterone from birth to pubertal age in beef bulls. Theriogenology. 2011; 76:1632–1638. doi: 10.1016/j.theriogenology.2011.07.011 21872311

22. Satchell L, Glister C, Bleach EC, Glencross RG, Bicknell AB, Dai Yet al. Ovarian expression of insulin-like peptide 3 (INSL3) and its receptor (RXFP2) during development of bovine antral follicles and corpora lutea and measurement of circulating INSL3 levels during synchronized estrous cycles. Endocrinology. 2013; 154:1897–1906. doi: 10.1210/en.2012-2232 23546605

23. Pitia AM, Uchiyama K, Sano H, Kinukawa M, Minato Y, Sasada H et al. Functional insulin-like factor 3 (INSL3) hormone-receptor system in the testes and spermatozoa of domestic ruminants and its potential as a predictor of sire fertility. Anim Sci J. 2017; 88:678–690. doi: 10.1111/asj.12694 27592693

24. Sakase M, Kitagawa K, Kibushi M, Kawate N, Weerakoon WWPN, Hannan MA et al. Relationships of plasma insulin-like peptide 3, testosterone, inhibin, and insulin-like growth factor-I concentrations with scrotal circumference and testicular weight in Japanese Black beef bull calves. J Reprod Dev. 2018; 64:401–407. doi: 10.1262/jrd.2018-034 29984734

25. Byrne CJ, Fair S, English AM, Urh C, Sauerwein H, Crowe MA et al. Plane of nutrition before and after 6 months of age in Holstein-Friesian bulls: II. Effects on metabolic and reproductive endocrinology and identification of physiological markers of puberty and sexual maturation. J Dairy Sci. 2018; 101:3460–3475. doi: 10.3168/jds.2017-13720 29397166

26. Anand-Ivell R, Hiendleder S, Viñoles C, Martin GB, Fitzsimmons C, Eurich A et al. INSL3 in the ruminant: a powerful indicator of gender- and genetic-specific feto-maternal dialogue. PLOS One. 2011; 6:e19821. doi: 10.1371/journal.pone.0019821 21603619

27. Beltman ME, Forde N, Furney P, Carter F, Roche JF, Lonergan P et al. Characterisation of endometrial gene expression and metabolic parameters in beef heifers yielding viable or non-viable embryos on Day 7 after insemination. Rep Fertil Dev. 2010; 22:987–999.

28. Crowe MA, Padmanabhan V, Hynes N, Sunderland SJ, Enright WJ, Beitins IZ et al. Validation of a sensitive radioimmunoassay to measure serum follicle-stimulating hormone in cattle: correlation with biological activity. Anim Reprod Sci. 1997; 48:123–136. doi: 10.1016/s0378-4320(97)00022-5 9452868

29. Cooke DJ, Crowe MA, Roche JF. Circulating FSH isoform patterns during recurrent increases in FSH throughout the oestrous cycle of heifers. J Reprod Fert. 1997; 110:339–345.

30. Collodel G, Moretti E, Del Vecchio MT, Biagi M, Cardinali R, Mazzi L et al. Effect of chocolate and Propolfenol on rabbit spermatogenesis and sperm quality following bacterial lipopolysaccharide treatment. Syst Biol Reprod Med. 2014; 60:217–226. doi: 10.3109/19396368.2014.911392 24785944

31. RRID:AB_2800359, https://scicrunch.org/resolver/AB_2800359

32. Ferlin A, Garolla A, Rigon F, Rasi Caldogno L, Lenzi A, Foresta C. Changes in serum insulin-like factor 3 during normal male puberty. J Clin Endocrinol Metab. 2006; 91:3426–3431. doi: 10.1210/jc.2006-0821 16804040

33. Wikström AM, Bay K, Hero M, Andersson AM, Dunkel L. Serum insulin-like factor 3 levels during puberty in healthy boys and boys with Klinefelter syndrome. J Clin Endocrinol Metab. 2006; 91:4705–4708. doi: 10.1210/jc.2006-0669 16926256

34. Johansen ML, Anand-Ivell R, Mouritsen A, Hagen CP, Mieritz MG, Søeborg T et al. Serum levels of Insulin-like factor 3, Anti-Müllerian Hormone, Inhibin B and Testosterone during pubertal transition in healthy boys: a longitudinal pilot study. Reproduction. 2014; 147:529–535. doi: 10.1530/REP-13-0435 24459206

35. Minagawa I, Sagata D, Pitia AM, Kohriki H, Shibata M, Sasada H et al. Dynamics of insulin-like factor 3 and its receptor expression in boar testes. J Endocrinol. 2014; 220:247–261. doi: 10.1530/JOE-13-0430 24464024

36. Hannan MA, Kawate N, Fukami Y, Weerakoon WWPN, Büllesbach EE, Inaba T et al. Changes of plasma concentrations of insulin-like peptide 3 and testosterone, and their association with scrotal circumference during pubertal development in male goats. Theriogenology. 2017; 92:51–56. doi: 10.1016/j.theriogenology.2017.01.009 28237342

37. Weerakoon WWPN, Sakase M, Kawate N, Hannan MA, Kohama N, Tamada H. Plasma IGF-I, INSL3, testosterone, inhibin concentrations and scrotal circumferences surrounding puberty in Japanese Black beef bulls with normal and abnormal semen. Theriogenology. 2018; 114:54–62. doi: 10.1016/j.theriogenology.2018.03.006 29597124

38. Hombach-Klonisch S, Schön J, Kehlen A, Blottner S, Klonisch T. Seasonal expression of INSL3 and Lgr8/Insl3 receptor transcripts indicates variable differentiation of Leydig cells in the roe deer testis. Biol Reprod. 2004; 71:1079–1087. doi: 10.1095/biolreprod.103.024752 15151926

39. Heng K, Anand-Ivell R, Teerds K, Ivell R. The endocrine disruptors dibutyl phthalate (DBP) and diethylstilbestrol (DES) influence Leydig cell regeneration following ethane dimethane sulfonate (EDS) treatment of adult male rats. Int J Androl. 2012; 35:353–363. doi: 10.1111/j.1365-2605.2011.01231.x 22150342

40. Anand-Ivell RJK, Relan V, Balvers M, Fritsch M, Bathgate RAD, Ivell R. Expression of the Insulin-like peptide 3 (INSL3) hormone-receptor (LGR8) system in the testis. Biol Reprod. 2006; 74:945–953. doi: 10.1095/biolreprod.105.048165 16467492

41. Del Borgo MP, Hughes RA, Bathgate RA, Lin F, Kawamura K, Wade JD. Analogs of insulin-like peptide 3 (INSL3) B-chain are LGR8 antagonists in vitro and in vivo. J Biol Chem. 2006; 281:13068–13074. doi: 10.1074/jbc.M600472200 16547350

42. Minagawa I, Murata Y, Terada K, Shibata M, Park EY, Sasada H et al. Evidence for the role of INSL3 on sperm production in boars by passive immunisation. Andrologia. 2018; 50:e13010. doi: 10.1111/and.13010 29575065

43. Amory JK, Page ST, Anawalt BD, Coviello AD, Matsumoto AM, Bremner WJ. Elevated end-of-treatment serum INSL3 is associated with failure to completely suppress spermatogenesis in men receiving male hormonal contraception. J Androl. 2007; 28:548–554. doi: 10.2164/jandrol.106.002345 17314233

44. Abbitt B, Fiske RA, Craig TM, Bitter JW. Scrotal hydrocele secondary to ascites in 28 bulls. J Am Vet Med Assoc. 1995; 207:753–756. 7657577

45. Barth AD. The use of bull breeding soundness evaluation to identify subfertile and infertile bulls. Animal. 2018; 12:s158–s164. doi: 10.1017/S1751731118000538 29560847

46. English AM, Byrne CJ, Cormican P, Waters SM, Fair S, Kenny DA. Effect of early calf-hood nutrition on the transcriptional regulation of the hypothalamic-pituitary-testicular axis in Holstein-Friesian bull calves. Sci Rep. 2018; 8:16577. doi: 10.1038/s41598-018-34611-4 30409985

47. Castilla-Cortázar I, Gago A, Muñoz Ú, Ávila-Gallego E, Guerra-Menéndez L, Sádaba MC et al. Mechanisms underlying testicular damage and dysfunction in mice with partial IGF-1 deficiency and the effectiveness of IGF-1 replacement therapy. Urology. 2015; 86:1241.e1-9.

Prepubertal nutrition alters Leydig cell functional capacity and timing of puberty

Souhrn

Klíčová slova:

Zdroje

PLOS One

INSIGHTS from European Respiratory Congress

Současné pohledy na riziko v parodontologii

Svět praktické medicíny 3/2024 (znalostní test z časopisu)

Kardiologické projevy hypereozinofilií

Střevní příprava před kolonoskopií