The influence of nutrition on the insulin-like growth factor system and the concentrations of growth hormone, glucose, insulin, gonadotropins and progesterone in ovarian follicular fluid and plasma from adult female horses (Equus caballus)

Reproductive Biology and Endocrinology

Volumn 12, Issue 1, 2014, Pages

  Salazar Ortiz, Juan ^a,b,c   Monget, Philippe ^a,b,c   Guillaume, Daniel ^a,b,c  

^a UMR85 PHYSIOLOGIE DE LA REPRODUCTION ET DES COMPORTEMENTS   (France)

^b UNIVERSITÉ DE TOURS   (France)

^c IFCE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

FOLLITROPIN; GLUCOSE; GONADOTROPIN; GROWTH HORMONE; INSULIN; LUTEINIZING HORMONE; PROGESTERONE; SOMATOMEDIN; SOMATOMEDIN B; SOMATOMEDIN C; GLUCOSE BLOOD LEVEL; INSULIN DERIVATIVE; SERIC GONADOTROPIN; SOMATOMEDIN BINDING PROTEIN; SOMATOMEDIN BINDING PROTEIN 3;

ADULT; ANIMAL EXPERIMENT; ARTICLE; BLOOD LEVEL; BLOOD SAMPLING; BODY WEIGHT; CONTROLLED STUDY; CORPUS LUTEUM; DIET RESTRICTION; DOMESTIC HORSE; ECHOGRAPHY; FEMALE; FOLLICULAR ASPIRATION; FOLLITROPIN BLOOD LEVEL; GLUCOSE BLOOD LEVEL; GONADOTROPIN BLOOD LEVEL; GROWTH HORMONE BLOOD LEVEL; INSULIN BLOOD LEVEL; LIMIT OF QUANTITATION; LUTEINIZING HORMONE BLOOD LEVEL; LUTEINIZING HORMONE RELEASE; NONHUMAN; NUTRITION; OVARY FOLLICLE FLUID; OVULATION; PROGESTERONE BLOOD LEVEL; PROTEIN BLOOD LEVEL; PUNCTURE; RADIOIMMUNOASSAY; SUBCUTANEOUS FAT; WESTERN BLOTTING; ADVERSE EFFECTS; ANALYSIS; ANIMAL; BLOOD; CALORIC RESTRICTION; CHEMISTRY; FRANCE; GROWTH, DEVELOPMENT AND AGING; HORSE; METABOLISM; OVARY FOLLICLE; PHYSIOLOGY; PROESTRUS; RANDOMIZED CONTROLLED TRIAL; SECRETION (PROCESS); SIGNAL TRANSDUCTION; VETERINARY;

EQUIDAE; EQUUS CABALLUS;

ANIMALS; BLOOD GLUCOSE; CALORIC RESTRICTION; FEMALE; FOLLICULAR FLUID; FRANCE; GLUCOSE; GONADOTROPINS, EQUINE; GROWTH HORMONE; HORSES; INSULIN-LIKE GROWTH FACTOR BINDING PROTEIN 3; INSULIN-LIKE GROWTH FACTOR BINDING PROTEINS; INSULIN-LIKE GROWTH FACTOR I; INSULIN-LIKE GROWTH FACTOR II; INSULINS; OVARIAN FOLLICLE; PROESTRUS; PROGESTERONE; SIGNAL TRANSDUCTION;

EID: 84908060193     PISSN: None     EISSN: 14777827     Source Type: Journal    
DOI: 10.1186/1477-7827-12-72     Document Type: Article

References (66)

1. Briant C, Ottogalli M, Morel M, Guillaume D. Use of GnRH antagonist, antarelix, associated or not with hCG, to control ovulation in cyclic pony mares. Domest Anim Endocrinol 2003, 24:305-322.
2. Gérard N, Loiseau S, Duchamp G, Seguin F. Analysis of the variations of follicular fluid composition during follicular growth and maturation in the mare using proton nuclear magnetic resonance (1H NMR). Reproduction 2002, 124:241-248.
3. Guillaume D, Bruneau B, Briant C. Comparison of the effects of two GnRH antagonists on LH and FSH secretion, follicular growth and ovulation in the mares. Reprod Nutr Dev 2002, 42:251-264.
4. Nagy P, Huszenicza G, Reiczigel J, Juhász J, Palmer E, Kulcsár M, Abaváry K, Guillaume D. Factors affecting plasma progesterone concentration and the retrospective determination of the time of ovulation in cyclic mares. Theriogenology 2004, 61:203-214.
5. Gérard N, Prades A, Couty I, Labberte M, Daels P, Duchamp G. Follicular fluid concentrations of glucose, pyruvate and lactate in relation to follicular growth, preovulatory maturation and oocyte nuclear maturation stage in the mare. Theriogenology, Annual Conference of the International Embryo Transfer Society, Volume 53 2000, 9-11. Maastricht: Janvier, Abst p:372.
6. Spicer LJ, Echternkamp SE. The ovarian insulin and insulin-like growth factor system with an emphasis on domestic animals. Dom Anim Endocrinol 1995, 12:223-245.
7. Beg MA, Ginther OJ. Follicle selection in cattle and horses: role of intrafollicular factors. Reproduction 2006, 132:365-377.
8. Salazar-Ortiz J, Camous S, Briant C, Lardic L, Chesneau D, Guillaume D. Effects of nutritional cues on the duration of the winter anovulatory phase and on associated hormone levels in adult female Welsh pony horses (Equus caballus). Reprod Biol Endocrinol 2011, 9:130-146.
9. Gastal MO, Gastal EL, Spinelli V, Ginther OJ. Relationships between body condition and follicle development in mares. Anim Reprod 2004, 1:115-121.
10. Salazar-Ortiz J, Audouin E, Delpuech T, Monget P, Guillaume D. Effet du niveau d'alimentation sur la croissance folliculaire et certains taux hormonaux plasmatiques de la jument. 30ème Journée de la Recherche Equine 2004, France: Eds Les Haras Nationaux Paris.
11. Silva JR, Figueiredo JR, Van Den Hurk R. Involvement of growth hormone (GH) and insulin-like growth factor (IGF) system in ovarian folliculogenesis. Theriogenology 2009, 71:1193-1208.
12. Armstrong DG, McEvoy TG, Baxter G, Robinson JJ, Hogg CO, Woad KJ, Webb R, Sinclair KD. Effect of dietary energy and protein on bovine follicular dynamics and embryo production in vitro: associations with the ovarian insulin-like growth factor system. Biol Reprod 2001, 64:1624-1632.
13. Mazerbourg S, Bondy CA, Zhou J, Monget P. The insulin-like growth factor system: a key determinant in the growth and selection of ovarian follicles? A comparative species study. Reprod Dom Anim 2003, 38:247-258.
14. Rivera GM, Fortune JE. Proteolysis of insulin-like growth factor binding proteins -4 and -5 in bovine follicular fluid: implications for ovarian follicular selection and dominance. Endocrinology 2003, 144:2977-2987.
15. Monget P, Mazerbourg S, Delpuech T, Maurel MC, Maniere S, Zapf J, Lalmanach G, Oxvig C, Overgaard MT. Pregnancy-associated plasma protein-A is involved in insulin-like growth factor binding protein-2 (IGFBP-2) proteolytic degradation in bovine and porcine preovulatory follicles: identification of cleavage site and characterization of IGFBP-2 degradation. Biol Reprod 2003, 68:77-86.
16. Gérard N, Delpuech T, Oxvig C, Overgaard MT, Monget P. Proteolytic degradation of IGF-binding protein (IGFBP)-2 in equine ovarian follicles: involvement of pregnancy-associated plasma protein-A (PAPP-A) and association with dominant but not subordinated follicles. J Endocrinol 2004, 182:457-466.
17. Mazerbourg S, Overgaard MT, Oxvig C, Christiansen M, Conover CA, Laurendeau I, Vidaud M, Tosser-Klopp G, Zapf J, Monget P. Pregnancy-associated plasma protein-A (PAPP-A) in ovine, bovine, porcine, and equine ovarian follicles: involvement in IGF binding protein-4 proteolytic degradation and mRNA expression during follicular development. Endocrinology 2001, 142:5243-5253.
18. Santiago CA, Voge JL, Aad PY, Allen DT, Stein DR, Malayer JR, Spicer LJ. Pregnancy-associated plasma protein-A and insulin-like growth factor binding protein mRNAs in granulosa cells of dominant and subordinate follicles of preovulatory cattle. Domest Anim Endocrinol 2005, 28:46-63.
19. Butler ST, Marr AL, Pelton SH, Radcliff RP, Lucy MC, Butler WR. Insulin restores GH responsiveness during lactation-induced negative energy balance in dairy cattle: effects on expression of IGF-I and GH receptor 1A. J Endocrinol 2003, 176:205-217.
20. Lubbers ER, List EO, Jara A, Sackman-Sala L, Cordoba-Chacon J, Gahete MD, Kineman RD, Ravneet Boparai RB, Bartke A, Kopchick JJ, Berryman DE. Adiponectin in mice with altered GH action: links to insulin sensitivity and longevity?. J Endocrinol 2013, 216:363-374.
21. Ginther OJ, Gastal EL, Gastal MO, Siddiqui MAR, Beg MA. Relationships of follicle versus oocyte maturity to ultrasound morphology, blood flow, and hormone concentrations of the preovulatory follicle in mares. Biol Reprod 2007, 77:202-208.
22. Marchal R, Caillaud M, Martoriati A, Gérard N, Mermillod P, Goudet G. Effect of growth hormone (GH) on in vitro nuclear and cytoplasmic oocyte maturation, cumulus expansion, hyaluronan synthases, and connexins 32 and 43 expression, and GH receptor messenger RNA expression in equine and porcine species. Biol Reprod 2003, 69:1013-1022.
23. Pereira GR, Lorenzo PL, Carneiro GF, Ball BA, Pegoraro LMC, Pimentel CA, Liu IKM. Influence of equine growth hormone, insulin-like growth factor-I and its interaction with gonadotropins on in vitro maturation and cytoskeleton morphology in equine oocytes. Animal 2013, 7:1493-1499.
24. INRA HN, IE Notation de l'état corporel des chevaux de selle et de sport. Guide pratique 1997, Paris: Eds Institut Elevage Publishing, INRA HN, IE.
25. Duchamp G, Bézard J, Palmer E. Oocyte yield and consequences of puncture of all follicles larger than 8 millimeters in mares. In 'Equine Reproduction VI'. Biol Reprod, Monograph series 1995, 1:233-241.
26. Monget P, Monniaux D, Pisselet C, Durand P. Changes in insulin-like growth factor-I (IGF-1), IGF-1I, and their binding proteins during growth and atresia of ovine ovarian follicles. Endocrinology 1993, 132:1438-1446.
27. Hossenlopp P, Seurin D, Segovia-Quinson B, Hardouin S, Binoux M. Analysis of serum insulin-like growth factor binding proteins using western blotting: use of the method for titration of the binding proteins and competitive binding studies. Anal Biochem 1986, 154:138-143.
28. Little RC, Henry PR, Ammerman CB. Statistical analysis of repeated measures data using SAS procedures. J Anim Sci 1998, 76:1216-1231.
29. Dominguez MM. Effects of body condition, reproductive status and breed on follicular population and oocyte quality in cows. Theriogenology 1995, 43:1405-1418.
30. Kendrick KW, Bailey TL, Garst AS, Pryor AW, Ahmadzadeh A, Akers RM, Eyestone WE, Pearson RE, Gwazdauskas FC. Effects of energy balance of hormones, ovarian activity, and recovered oocytes in lactating Holstein cows using transvaginal follicular aspiration. J Dairy Sci 1999, 82:1731-1741.
31. Gutiérrez CG, Oldham J, Bramley TA, Gong JG, Campbell BK, Webb R. The recruitment of ovarian follicles is enhanced by increased dietary intake in heifers. J Anim Sci 1997, 75:1876-1884.
32. Gong JG. Influence of metabolic hormones and nutrition on ovarian follicle development in cattle: practical implications. Dom Anim Endocr 2002, 23:229-241.
33. Downing JA, Scaramuzzi RJ. Nutrient effects on ovulation rate, ovarian function and the secretion of gonadotrophic and metabolic hormones in sheep. J Reprod Fertil Suppl 1991, 43:209-227.
34. Cox NM, Stuart MJ, Althen TG, Bennett WA, Miller HW. Enhancement of ovulation rate in gilts by increasing dietary energy and administering insulin during follicular growth. J Anim Sci 1987, 64:507-516.
35. Cochran RA, Leonardi-Cattolica AA, Sullivan MR, Kincaid LA, Leise BS, Thompson DL, Godke RA. The effects of equine somatotropin (eST) on follicular development and circulating plasma hormone profiles in cyclic mares treated during different stages of the estrous cycle. Domest Anim Endocrinol 1999, 16:57-67.
36. Peugnet P, Duchamp G, Reigner F, Dupont P, Barrey E, Guillaume D. Effect of growth hormone treatment on folicular growth in well-fed or feed restricted mares. Anim Reprod Sci 2010, 121S:S42-S44.
37. Landau S, Braw-Tal R, Kaim M, Bor A, Bruckental I. Preovulatory follicular status and diet affect the insulin and glucose content of follicles in high-yielding dairy cows. Anim Reprod Sci 2000, 64:181-197.
38. McClure TJ, Nancarrow CD, Radford HM. The effect of 2-deoxy-D-glucose on ovarian function of cattle. Aust J Biol Sci 1978, 31:183-186.
39. Gallet C, Dupont J, Campbell BK, Monniaux D, Guillaume D, Scaramuzzi RJ. The infusion of glucose in ewes during the luteal phase increases the number of follicles but reduces oestradiol production and some correlates of metabolic function in the large follicles. Anim Reprod Sci 2011, 127:154-163.
40. Poretsky L, Cataldo NA, Rosenwaks Z, Giudice LC. The insulin-related ovarian regulatory system in health and disease. Endocr Rev 1999, 20:535-582.
41. Quesnel H, Pasquier A, Jan N, Prunier A. Influence of insulin treatment and feed restriction on follicular development in cyclic gilts. Anim Reprod Sci 2000, 64:77-87.
42. Menassol JB, Collet A, Chesneau D, Malpaux B, Scaramuzzi RJ. The interaction between photoperiod and nutrition and its effects on seasonal rhythms of reproduction in the ewe. Biol Reprod 2012, 86:1-12.
43. Bossis I, Wettemann RP, Welty SD, Vizcarra JA, Spicer LJ, Diskin MG. Nutritionally induced anovulation in beef heifers: ovarian and endocrine function preceding cessation of ovulation. J Anim Sci 1999, 77:1536-1546.
44. Henry BA, Goding JW, Tilbrook AJ, Dunshea FR, Blache D, Clarke IJ. Leptin-mediated effects of undernutrition or fasting on luteinizing hormone and growth hormone secretion in ovariectomized ewes depend on the duration of metabolic perturbation. J Neuroendocrinol 2004, 16:244-255.
45. McManus CJ, Fitzgerald BP. Effects of a single day of feed restriction on changes in serum leptin, gonadotrophins, prolactin and metabolites in aged and young mares. Dom Anim Endocr 2000, 19:1-13.
46. Scacchi M, Pincelli AI, Cavagnini F. Nutritional status in the neuroendocrine control of growth hormone secretion: the model of anorexia nervosa. Front Neuroendocrinol 2003, 24:200-224.
47. Leung DW, Spencer SA, Cachianes G, Hammonds RG, Collins C, Henzel WJ, Barnard R, Waters MJ, Wood WI. Growth hormone receptor and serum binding protein: purification, cloning and expression. Nature 1987, 330:537-543.
48. Kelly PA, Djiane J, Postel-Vinay MC, Edery M. The prolactin/growth hormone receptor family. Endocr Rev 1991, 12:235-251.
49. Donaghy A, Ross R, Gimson A, Hughes SC, Holly J, Williams R. Growth hormone, insulin-like growth factor-1, and insulin-like growth factor binding proteins 1 and 3 in chronic liver disease. Hepatology 1995, 21:680-688.
50. Bartke A, Brown-Borg H. Life extension in the dwarf mouse. Curr Top Dev Biol 2004, 63:189-225.
51. Spicer LJ, Crowe MA, Prendiville DJ, Goulding D, Enricht WJ. Systematic but not ovarian concentrations of insulin-like growth factor-I are affected by short-term fasting. Biol Reprod 1992, 46:920-925.
52. Amstalden M, Garcia MR, Williams SW, Stanko RL, Nizielski SE, Morrison CD, Keisler DH, Williams GL. Leptin gene expression, circulating leptin, and luteinizing hormone pulsatility are acutely responsive to short-term fasting in prepubertal heifers: relationships to circulating insulin and insulin-like growth factor I(1). Biol Reprod 2000, 63:127-133.
53. Gentry LR, Thompson DL, Gentry GT, Davis KA, Godke RA, Cartmill JA. The relationship between body condition, leptin, and reproductive and hormonal characteristics of mares during the seasonal anovulatory period. J Anim Sci 2002, 80:2695-2703.
54. Watson ED, Bae SE, Thomassen R, Thomson SRM, Woad K, Armstrong DG. Insulin-like growth factors-I and -II and insulin-like growth factor-binding protein-2 in dominant equine follicles during spring transition and the ovulatory season. Reproduction 2004, 128:321-329.
55. Bridges TS, Davidson TR, Chamberlain CS, Geisert RD, Spicer LJ. Changes in FF steroids, insulin-like growth factors (IGF) and IGF-binding protein concentration, and proteolytic activity during equine follicular development. J Anim Sci 2002, 80:179-190.
56. Leeuwenberg BR, Hudson NL, Moore LG, Hurst PR, McNatty KP. Peripheral and ovarian IGF-I concentrations during the ovine oestrous cycle. J Endocrinol 1996, 148:281-289.
57. Besnard N, Pisselet C, Zapf J, Hornebeck W, Monniaux D, Monget P. Proteolytic activity is involved in changes in intrafollicular insulin-like growth factor-binding protein levels during growth and atresia of ovine ovarian follicles. Endocrinology 1996, 137:1599-1607.
58. Khalid M, Haresign W, Luck MR. Secretion of IGF-1 by ovine granulosa cells: effects of growth hormone and follicle stimulating hormone. Anim Reprod Sci 2000, 58:261-272.
59. Jones JI, Clemmons DR. Insulin-like growth factors and their binding proteins: biological actions. Endocr Rev 1995, 16:3-34.
60. Hodgkinson SC, Moore L, Napier JR, Davis SR, Bass JJ, Gluckman PD. Characterization of insulin-like growth factor binding proteins in ovine tissue fluids. J Endocrinol 1989, 120:429-438.
61. Stanko RL, Cohick WS, Shaw DW, Harvey RW, Clemmons DR, Whitacre MD, Armstrong JD. Effect of somatotropin and/or equine chorionic gonadotropin on serum and follicular insulin-like growth factor I and insulin-like growth factor binding proteins in cattle. Biol Reprod 1994, 50:290-300.
62. Oldham JM, Martyn JAK, Hua KM, MacDonald NA, Hodgkinson SC, Bass JJ. Nutritional regulation of IGF-2, but not IGF-1, is age dependent in sheep. J Endocrinol 1999, 163:395-402.
63. Prado TM, Wettemann RP, Spicer LJ, Vizcarra JA, Morgan GL. Influence of exogenous gonadotropin-releasing hormone on ovarian function in beef cows after short- and long-term nutritionally induced anovulation. J Anim Sci 2002, 80:3268-3276.
64. Boisclair YR, Rhoads RP, Ueki I, Wang J, Ooi GT. The acid-labile subunit (ALS) of the 150 kDa IGF-binding protein complex: an important but forgotten component of the circulating IGF system. J Endocrinol 2001, 170:63-70.
65. Hughes SC, Mason HD, Franks S, Holly JM. The insulin-like growth factors (IGFs) in follicular fluid are predominantly bound in the ternary complex. J Endocrinol 1997, 155:1-4.
66. Gérard N, Monget P. Intrafollicular Insulin-Like Growth Factor-Binding Protein Levels in Equine Ovarian Follicles during Preovulatory Maturation and Regression. Biol Reprod 1998, 58:1508-1514.