Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.
ADVANCED SEARCH
Log in
Top
Reproductive Biology and Endocrinology
Published in: Reproductive Biology and Endocrinology 1/2014

Open Access 01-12-2014 | Research

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)

Authors: Juan Salazar-Ortiz, Philippe Monget, Daniel Guillaume

Published in: Reproductive Biology and Endocrinology | Issue 1/2014

Login to get access

Abstract

Background

Feed intake affects the GH-IGF system and may be a key factor in determining the ovarian follicular growth rate. In fat mares, the plasma IGF-1 concentration is high with low GH and a quick follicular growth rate, in contrast to values observed in thin mares. Nothing is known regarding the long-term effects of differential feed intake on the IGF system. The objective of this experiment was to quantify IGFs, IGFBPs, GH, glucose, insulin, gonadotropin and progesterone (P4) in blood and in preovulatory follicular fluid (FF) in relation to feeding levels in mares.

Methods

Three years prior to the experiment, Welsh Pony mares were assigned to a restricted diet group (R, n = 10) or a well-fed group (WF, n = 9). All mares were in good health and exhibited differences in body weight and subcutaneous fat thickness. Follicular development was scanned daily and plasma was also collected daily. Preovulatory FF was collected by ultrasound-guided follicular aspiration. Hormone levels were assayed in FF and plasma with a validated RIA.

Results

According to scans, the total number of follicles in group R was 53% lower than group WF. Insulin and IGF-1 concentrations were higher in WF than in R mares. GH and IGF-2 concentrations were lower in plasma from WF mares than from R mares, but the difference was not significant in FF. The IGFBP-2/IGFBP-3 ratio in FF was not affected by feeding but was dramatically increased in R mare plasma. No difference in gonadotropin concentration was found with the exception of FSH, which was higher in the plasma of R mares. On the day of puncture, P4 concentrations were not affected by feeding but were higher in preovulatory FF than in plasma.

Conclusions

The bioavailability of IGF-1 or IGF-2, represented by the IGFBP2/IGFBP3 ratio, is modified by feed intake in plasma but not in FF. These differences partially explain the variability in follicular growth observed between well-fed mares and mares on restricted diets.
Appendix
Available only for authorised users
Literature
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.CrossRefPubMed
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.CrossRefPubMed
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.CrossRefPubMed
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.CrossRefPubMed
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, Maastricht: Janvier, 9-11. 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.CrossRef
7.
Beg MA, Ginther OJ: Follicle selection in cattle and horses: role of intrafollicular factors. Reproduction. 2006, 132: 365-377.CrossRefPubMed
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.PubMedCentralCrossRefPubMed
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.CrossRefPubMed
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.CrossRefPubMed
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.CrossRef
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.CrossRefPubMed
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.CrossRefPubMed
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.CrossRefPubMed
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.CrossRefPubMed
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.CrossRefPubMed
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.CrossRefPubMed
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.PubMedCentralCrossRefPubMed
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.CrossRefPubMed
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.CrossRefPubMed
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.CrossRefPubMed
24.
INRA HN, IE: Notation de l’état corporel des chevaux de selle et de sport. Guide pratique. 1997, Paris: Eds Institut Elevage Publishing
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.PubMed
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.CrossRefPubMed
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.CrossRef
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.CrossRefPubMed
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.PubMed
32.
Gong JG: Influence of metabolic hormones and nutrition on ovarian follicle development in cattle: practical implications. Dom Anim Endocr. 2002, 23: 229-241.CrossRef
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.PubMed
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.PubMed
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.CrossRefPubMed
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.CrossRefPubMed
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.PubMed
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.CrossRefPubMed
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.CrossRefPubMed
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.CrossRefPubMed
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.PubMed
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.CrossRefPubMed
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.CrossRef
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.CrossRefPubMed
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.CrossRefPubMed
48.
Kelly PA, Djiane J, Postel-Vinay MC, Edery M: The prolactin/growth hormone receptor family. Endocr Rev. 1991, 12: 235-251.CrossRefPubMed
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.PubMed
50.
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.CrossRefPubMed
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.CrossRefPubMed
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.PubMed
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.CrossRefPubMed
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.PubMed
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.CrossRefPubMed
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.PubMed
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.CrossRefPubMed
59.
Jones JI, Clemmons DR: Insulin-like growth factors and their binding proteins: biological actions. Endocr Rev. 1995, 16: 3-34.PubMed
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.CrossRefPubMed
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.CrossRefPubMed
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.CrossRefPubMed
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.PubMed
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.CrossRefPubMed
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.CrossRef
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.CrossRefPubMed
Metadata
Title
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)
Authors
Juan Salazar-Ortiz
Philippe Monget
Daniel Guillaume
Publication date
01-12-2014
Publisher
BioMed Central
Published in
Reproductive Biology and Endocrinology / Issue 1/2014
Electronic ISSN: 1477-7827
DOI
https://doi.org/10.1186/1477-7827-12-72

Other articles of this Issue 1/2014

Reproductive Biology and Endocrinology 1/2014 Go to the issue

Research

Wisteria floribunda agglutinin-binding glycan expression is decreased in endometriomata

Hypothesis

Management of long-term and reversible hysteroscopic sterilization: a novel device with nickel-titanium shape memory alloy

Research

Comparing two different superovulation protocols on ovarian activity and fecal glucocorticoid levels in the brown brocket deer (Mazama gouazoubira)

Debate

Is it time to shift the attention on early stages embryo development to avoid inconclusive evidence on HPV-related infertility: debate and proposal

Research

Endometrial beta3 Integrin profile reflects endometrial receptivity defects in women with unexplained recurrent pregnancy loss

Research

The effect of hormonal estrus induction on maternal effect and apoptosis-related genes expression in porcine cumulus-oocyte complexes