Early starvation in European seabass (Dicentrarchus labrax) larvae has no drastic effect on hepatic intermediary metabolism in juveniles.

Arginine vasotocin Early fasting Fish Metabolic programming

Journal

Fish physiology and biochemistry
ISSN: 1573-5168
Titre abrégé: Fish Physiol Biochem
Pays: Netherlands
ID NLM: 100955049

Informations de publication

Date de publication:
17 Feb 2024
Historique:
received: 13 11 2023
accepted: 10 02 2024
medline: 17 2 2024
pubmed: 17 2 2024
entrez: 17 2 2024
Statut: aheadofprint

Résumé

The present study aims to investigate nutritional programming through early starvation in the European seabass (Dicentrarchus labrax). European seabass larvae were fasted at three different developmental periods for three durations from 60 to 65 dph (F1), 81 to 87 dph (F2), and 123 to 133 dph (F3). Immediate effects were investigated by studying gene expression of npy (neuropeptide Y) and avt (Arginine vasotocin) in the head, while potential long-term effects (i.e., programming) were evaluated on intermediary metabolism later in life (in juveniles). Our findings indicate a direct effect regarding gene expression in the head only for F1, with higher avt mRNA level in fasted larved compared to controls. The early starvation periods had no long-term effect on growth performance (body weight and body length). Regarding intermediary metabolism, we analyzed related key plasma metabolites which reflect the intermediary metabolism: no differences for glucose, triglycerides, and free fatty acids in the plasma were observed in juveniles irrespective of the three early starvation stimuli. As programming is mainly linked to molecular mechanisms, we then studied hepatic mRNA levels for 23 key actors of glucose, lipid, amino acid, and energy metabolism. For many of the metabolic genes, there was no impact of early starvation in juveniles, except for three genes involved in glucose metabolism (glut2-glucose transporter and pk-pyruvate kinase) and lipid metabolism (acly-ATP citrate lyase) which were higher in F2 compared to control. Together, these results highlight that starvation between 81 to 87 dph may have more long-term impact, suggesting the existence of a developmental window for programming by starvation. In conclusion, European seabass appeared to be resilient to early starvation during larvae stages without drastic impacts on intermediary metabolism later in life.

Identifiants

pubmed: 38367082
doi: 10.1007/s10695-024-01320-x
pii: 10.1007/s10695-024-01320-x
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2024. The Author(s), under exclusive licence to Springer Nature B.V.

Références

Alliot E, Djabali M, Pastoureaud A, Thebault H (1984) Changes in the biochemical composition of tissues in Juvenile Sea bass during forced starvation. Biochem Syst Ecol 12:209–213. https://doi.org/10.1016/0305-1978(84)90038-3
doi: 10.1016/0305-1978(84)90038-3
Balment RJ, Lu W, Weybourne E, Warne JM (2006) Arginine vasotocin a key hormone in fish physiology and behaviour: a review with insights from mammalian models. Gen Comp Endocrinol 147:9–16. https://doi.org/10.1016/j.ygcen.2005.12.022
doi: 10.1016/j.ygcen.2005.12.022 pubmed: 16480986
Bezault E, Clota F, Derivaz M et al (2007) Sex determination and temperature-induced sex differentiation in three natural populations of Nile tilapia (Oreochromis niloticus) adapted to extreme temperature conditions. Aquaculture 272:S3–S16. https://doi.org/10.1016/j.aquaculture.2007.07.227
doi: 10.1016/j.aquaculture.2007.07.227
Caruso G, Denaro MG, Caruso R et al (2011) Response to short term starvation of growth, haematological, biochemical and non-specific immune parameters in European sea bass (Dicentrarchus labrax) and blackspot sea bream (Pagellus bogaraveo). Mar Environ Res 72:46–52. https://doi.org/10.1016/j.marenvres.2011.04.005
doi: 10.1016/j.marenvres.2011.04.005 pubmed: 21664688
Chatzifotis S, Papadaki M, Despoti S et al (2011) Effect of starvation and re-feeding on reproductive indices, body weight, plasma metabolites and oxidative enzymes of sea bass (Dicentrarchus labrax). Aquaculture 316:53–59. https://doi.org/10.1016/j.aquaculture.2011.02.044
doi: 10.1016/j.aquaculture.2011.02.044
Daulé S, Vandeputte M, Vergnet A et al (2014) Effect of selection for fasting tolerance on feed intake, growth and feed efficiency in the European sea bass Dicentrarchus labrax. Aquaculture 420–421:S42–S49. https://doi.org/10.1016/j.aquaculture.2013.05.036
doi: 10.1016/j.aquaculture.2013.05.036
Demmelmair H, von Rosen J, Koletzko B (2006) Long-term consequences of early nutrition. Early Human Dev 82:567–574. https://doi.org/10.1016/j.earlhumdev.2006.07.004
doi: 10.1016/j.earlhumdev.2006.07.004
Edwards PD, Lavergne SG, McCaw LK et al (2021) Maternal effects in mammals: Broadening our understanding of offspring programming. Front Neuroendocrinol 62:100924. https://doi.org/10.1016/j.yfrne.2021.100924
doi: 10.1016/j.yfrne.2021.100924 pubmed: 33992652
Fernandez-Twinn DS, Ozanne SE (2010) Early life nutrition and metabolic programming. Ann N Y Acad Sci 1212:78–96. https://doi.org/10.1111/j.1749-6632.2010.05798.x
doi: 10.1111/j.1749-6632.2010.05798.x pubmed: 21070247
Geffroy B, Gesto M, Clota F et al (2021) Parental selection for growth and early-life low stocking density increase the female-to-male ratio in European sea bass. Sci Rep 11:13620. https://doi.org/10.1038/s41598-021-93116-9
doi: 10.1038/s41598-021-93116-9 pubmed: 34193934 pmcid: 8245542
Gesto M, López-Patiño MA, Hernández J, et al (2013) The response of brain serotonergic and dopaminergic systems to an acute stressor in rainbow trout: a time-course study. J Exp Biol jeb.091751. https://doi.org/10.1242/jeb.091751
Geurden I, Borchert P, Balasubramanian M, Schrama JW, Dupont-Nivet M et al (2013) The positive impact of the early-feeding of a plant-based diet on its future acceptance and utilisation in rainbow trout. PLoS One 8(12):e83162. https://doi.org/10.1371/journal.pone.0083162
doi: 10.1371/journal.pone.0083162 pubmed: 24386155 pmcid: 3873907
Gilchriest BJ, Tipping DR, Hake L et al (2000) The effects of acute and chronic stresses on vasotocin gene transcripts in the brain of the rainbow trout (Oncorhynchus mykiss). J Neuroendocrinol 12:795–801. https://doi.org/10.1046/j.1365-2826.2000.00522.x
doi: 10.1046/j.1365-2826.2000.00522.x pubmed: 10929092
Good BJ (1993) Medicine, rationality and experience: an anthropological perspective. Cambridge University Press
doi: 10.1017/CBO9780511811029
Good CA, Kramer H, Somogyi M (1933) The determination of glycogen. J Biol Chem 100:485–491
doi: 10.1016/S0021-9258(18)75966-8
Gutiérrez J, Pérez J, Navarro I et al (1991) Changes in plasma glucagon and insulin associated with fasting in sea bass (Dicentrarchus labrax). Fish Physiol Biochem 9:107–112. https://doi.org/10.1007/BF02265126
doi: 10.1007/BF02265126 pubmed: 24214669
Hilge V (1985) The influence of temperature on the growth of the European catfish (Silurus glanis L.). J Appl Ichthyol 1:27–31. https://doi.org/10.1111/j.1439-0426.1985.tb00407.x
doi: 10.1111/j.1439-0426.1985.tb00407.x
Hou Z, Fuiman LA (2020) Nutritional programming in fishes: insights from mammalian studies. Rev Fish Biol Fisheries 30:67–92. https://doi.org/10.1007/s11160-019-09590-y
doi: 10.1007/s11160-019-09590-y
Hung SSO, Liu W, Li H et al (1997) Effect of starvation on some morphological and biochemical parameters in white sturgeon, Acipenser transmontanus. Aquaculture 151:357–363. https://doi.org/10.1016/S0044-8486(96)01506-2
doi: 10.1016/S0044-8486(96)01506-2
Koletzko B, Brands B, Poston L, Godfrey K, Demmelmair H (2012) Early nutrition programming of long-term health. Early Nutrition Project. Proc Nutr Soc. 71(3):371–8. https://doi.org/10.1017/S0029665112000596
Kumkhong S, Marandel L, Plagnes-Juan E et al (2021) Glucose injection into the yolk influences intermediary metabolism in adult Nile tilapia fed with high levels of carbohydrates. Animal 15:100347. https://doi.org/10.1016/j.animal.2021.100347
doi: 10.1016/j.animal.2021.100347 pubmed: 34455154
Kumkhong S, Marandel L, Plagnes-Juan E, Veron V, Boonanuntanasarn S, Panserat S (2020) Glucose injection into yolk positively modulates intermediary metabolism and growth performance in juvenile nile tilapia (Oreochromis niloticus). Front Physiol 11:286. https://doi.org/10.3389/fphys.2020.00286
Lall SP, Dumas A (2022) 3 - Nutritional requirements of cultured fish: formulating nutritionally adequate feeds. In: Davis DA (ed) Feed and Feeding Practices in Aquaculture, 2nd edn. Woodhead Publishing, Oxford, pp 65–132
doi: 10.1016/B978-0-12-821598-2.00005-9
Lucas A (1998) Programming by early nutrition: an experimental approach. J Nutr 128:401S-406S. https://doi.org/10.1093/jn/128.2.401S
doi: 10.1093/jn/128.2.401S pubmed: 9478036
Lucas A (2007) Programming by early nutrition in man. In: Ciba Foundation Symposium 156 - The Childhood Environment and Adult Disease. Wiley, Ltd, pp 38–55
Mancera JM, Vargas-Chacoff L, García-López A et al (2008) High density and food deprivation affect arginine vasotocin, isotocin and melatonin in gilthead sea bream (Sparus auratus). Comp Biochem Physiol a: Mol Integr Physiol 149:92–97. https://doi.org/10.1016/j.cbpa.2007.10.016
doi: 10.1016/j.cbpa.2007.10.016 pubmed: 18054261
Martins RST, Gomez A, Zanuy S, Carrillo M, Canario AVM (2015) Photoperiodic modulation of circadian clock and reproductive axis gene expression in the pre-pubertal European sea bass brain. PLoS One 10(12):e0144158. https://doi.org/10.1371/journal.pone.0144158
doi: 10.1371/journal.pone.0144158 pubmed: 26641263 pmcid: 4671726
Murphy BA, Fioramonti X, Jochnowitz N et al (2009a) Fasting enhances the response of arcuate neuropeptide Y-glucose-inhibited neurons to decreased extracellular glucose. Am J Physiol Cell Physiol 296:C746–C756. https://doi.org/10.1152/ajpcell.00641.2008
doi: 10.1152/ajpcell.00641.2008 pubmed: 19211911 pmcid: 2670660
Murphy KG, Wilcko MT, Wilcko WM, Ferguson DJ (2009b) Periodontal accelerated osteogenic orthodontics: a description of the surgical technique. J Oral Maxillofac Surg 67:2160–2166. https://doi.org/10.1016/j.joms.2009.04.124
doi: 10.1016/j.joms.2009.04.124 pubmed: 19761909
Navarro I, Gutiérrez J (1995) Chapter 17 fasting and starvation. In: Hochachka PW, Mommsen TP (eds) Biochemistry and Molecular Biology of Fishes. Elsevier, pp 393–434
Panserat S, Marandel L, Seiliez I, Skiba-Cassy S (2019) New insights on intermediary metabolism for a better understanding of nutrition in teleosts. Annu Rev Anim Biosci 7:195–220. https://doi.org/10.1146/annurev-animal-020518-115250
doi: 10.1146/annurev-animal-020518-115250 pubmed: 30418804
Pastoureaud A (1991) Influence of starvation at low temperatures on utilization of energy reserves, appetite recovery and growth character in sea bass, Dicentrarchus labrax. Aquaculture 99:167–178. https://doi.org/10.1016/0044-8486(91)90296-J
doi: 10.1016/0044-8486(91)90296-J
Sadoul B, Alfonso S, Bessa E, Bouchareb A, Blondeau-Bidet E, Clair P, Chatain B, Begout ML, Geffroy B (2018) Enhanced brain expression of genes related to cell proliferation and neural differentiation is associated with cortisol receptor expression in fishes. Gen Comp Endocrinol 267:76–81. https://doi.org/10.1016/j.ygcen.2018.06.001
doi: 10.1016/j.ygcen.2018.06.001 pubmed: 29902473
Shan X, Huang W, Cao L, Wu Y (2008) Advances in studies of the effects of starvation on growth and development of fish larvae. J Ocean Univ China 7:319–326. https://doi.org/10.1007/s11802-008-0319-3
doi: 10.1007/s11802-008-0319-3
Shimeno S, Shikata T, Hosokawa H et al (1997) Metabolic response to feeding rates in common carp, Cyprinus carpio. Aquaculture 151:371–377. https://doi.org/10.1016/S0044-8486(96)01492-5
doi: 10.1016/S0044-8486(96)01492-5
Silverstein JT, Breininger J, Baskin DG, Plisetskaya EM (1998) Neuropeptide Y-like gene expression in the salmon brain increases with fasting. Gen Comp Endocrinol 110(2):157–165. https://doi.org/10.1006/gcen.1998.7058
doi: 10.1006/gcen.1998.7058 pubmed: 9570936
Song Y, Alami-Durante H, Skiba-Cassy S et al (2019) Higher glycolytic capacities in muscle of carnivorous rainbow trout juveniles after high dietary carbohydrate stimulus at first feeding. Nutr Metab 16:77. https://doi.org/10.1186/s12986-019-0408-x
doi: 10.1186/s12986-019-0408-x
Srisakultiew N, Kumkhong S, Marandel L et al (2022) Short initial period of high carbohydrate feeding improves nutrient utilisation in juvenile Nile tilapia (Oreochromis niloticus) fed a high carbohydrate diet. Aquaculture 561:738661. https://doi.org/10.1016/j.aquaculture.2022.738661
doi: 10.1016/j.aquaculture.2022.738661
Stavrakidis-Zachou O, Papandroulakis N, Lika K (2019) A DEB model for European sea bass (Dicentrarchus labrax): parameterisation and application in aquaculture. J Sea Res 143:262–271. https://doi.org/10.1016/j.seares.2018.05.008
doi: 10.1016/j.seares.2018.05.008
Symonds ME, Sebert SP, Hyatt MA, Budge H (2009) Nutritional programming of the metabolic syndrome. Nat Rev Endocrinol 5:604–610. https://doi.org/10.1038/nrendo.2009.195
doi: 10.1038/nrendo.2009.195 pubmed: 19786987
Tolås I, Kalananthan T, Gomes AS, Lai F, Norland S, Murashita K, Rønnestad I (2021) Regional expression of npy mRNA paralogs in the brain of Atlantic salmon (Salmo salar, L.) and response to fasting. Front Physiol 12:720639. https://doi.org/10.3389/fphys.2021.720639
doi: 10.3389/fphys.2021.720639 pubmed: 34512390 pmcid: 8427667
Vagner M, Infante UZ, Robin JH, Person-Le Ruyet J (2007) Is it possible to influence European sea bass (Dicentrarchus labrax) juvenile metabolism by a nutritional conditioning during larval stage? 267(1–4):165–174. https://doi.org/10.1016/j.aquaculture.2007.01.031
Vandeputte M, Gagnaire P-A, Allal F (2019) The European sea bass: a key marine fish model in the wild and in aquaculture. Anim Genet 50:195–206. https://doi.org/10.1111/age.12779
doi: 10.1111/age.12779 pubmed: 30883830 pmcid: 6593706
Wang Y, Campbell JB, Kaftanoglu O et al (2016) Larval starvation improves metabolic response to adult starvation in honey bees (Apis mellifera L.). J Exp Biol 219:960–968. https://doi.org/10.1242/jeb.136374
doi: 10.1242/jeb.136374 pubmed: 27030776
Zambonino-Infante JL, Panserat S, Servili A et al (2019) Nutritional programming by dietary carbohydrates in European sea bass larvae: Not always what expected at juvenile stage. Aquaculture 501:441–447. https://doi.org/10.1016/j.aquaculture.2018.11.056
doi: 10.1016/j.aquaculture.2018.11.056

Auteurs

Khanakorn Phonsiri (K)

INRAE, Université de Pau Et Des Pays de L'Adour, NuMeA, Aquapôle, 64310, Saint-Pée-Sur-Nivelle, France.
School of School of Animal Technology and Innovation, Institute of Agricultural Technology, Suranaree University of Technology, 111 University Avenue, Tambon Suranaree, Muang, Nakhon Ratchasima, 30000, Thailand.

Benjamin Geffroy (B)

MARBEC, Université de Montpellier, 34095, Montpellier Cedex 05, France.

Jep Lokesh (J)

INRAE, Université de Pau Et Des Pays de L'Adour, NuMeA, Aquapôle, 64310, Saint-Pée-Sur-Nivelle, France.

Alexander Goikoetxea (A)

MARBEC, Université de Montpellier, 34095, Montpellier Cedex 05, France.

Sandrine Skiba-Cassy (S)

INRAE, Université de Pau Et Des Pays de L'Adour, NuMeA, Aquapôle, 64310, Saint-Pée-Sur-Nivelle, France.

Stephane Panserat (S)

INRAE, Université de Pau Et Des Pays de L'Adour, NuMeA, Aquapôle, 64310, Saint-Pée-Sur-Nivelle, France. stephane.panserat@inrae.fr.

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