Abstract
Plasma chemistry, lipid metabolism and vitellogenin gene expression of captive Sterlet sturgeon Acipenser ruthenus were studied in different maturity stages. A total of 32 fish were sampled, and maturity stages were identified on the basis of histological criteria and direct observation. Females were classified to four groups: previtellogenic, vitellogenic, post-vitellogenic, and atresia. Blood, gonad and liver tissue samples were taken through non-lethal biopsy. Our results showed that plasma levels of glucose, cholesterol, triacylglycerol, high-density lipoprotein, low-density lipoprotein, very low-density lipoprotein, calcium, phosphorus, alkaline phosphatase activity, albumin and total protein increased during ovarian development and were highest at post-vitellogenic stage. The lowest amounts in atresia stage demonstrate that lipid and energy imbalance was related to reabsorption and digestion of the yolk. These results suggested that the VLDL was the main plasma lipoprotein component of Sterlet. We determined that lipoprotein lipase and hepatic lipase activity increased during vitellogenesis process which suggested the role of lipase enzymes in regulating blood lipid metabolism. RT-PCR analysis indicates that Vitellogenin (VTG) mRNA could be detected both in livers and ovaries of female Sterlet. Throughout the study, the expression level of VTG gene showed an increase both in ovaries and in livers reaching its peak at late vitellogenesis stage. This strongly indicated a relation between VTG mRNA and ovarian development.
Similar content being viewed by others
References
Akhavan SR, Falahatkar B, ToloueiGilani MH, Lokman PM (2015) Effects of estradiol-17β implantation on ovarian growth, sex steroid levels and vitellogenin proxies in previtellogenic sturgeon Huso huso. Anim Rep Sci 157:1–10
Amiri BM, Maebayashi M, Hara A, Adachi S, Yamauchi K (1996) Ovarian development and serum sex steroid and vitellogenin profiles in the female cultured sturgeon hybrid, the bester. J Fish Biol 48:1164–1178
Ando S, Matsuzaki M (1996) A unique lipoprotein profile found in the plasma of cultured Japanese eel. Fish Physiol Biochem 15:469–479
Asadi F, Halajian A, Pourkabir M, Asadian P, Jadidizadeh F (2006) Serum biochemical parameters of Huso huso. Comp Clin Pathol 15:245–248
Babin PJ, Vernier JM (1989) Plasma lipoproteins in fish. J Lipid Res 30:467–489
Babin PJ, Boderg J, Kooiman FP, Van Marrewijk WJ, Van der Host DJ (1999) Apolipophorin II/I, apolipoprotein B, vitellogenin, and microsomal triglyceride transfer protein genes are derived from a common ancestor. J Mol Evol 49:150–160
Babin PJ, Cerdá J, Lubzens E (2007) The fish oocyte: from basic studies to biotechnological applications. Springer, The Netherlands
Baker ME (2002) Albumin, steroid hormones and the origin of vertebrates. J Endocrinol 175:121–127
Bidwell CA, Carlson DM (1995) Characterization of vitellogenin from white sturgeon, Acipenser transmontanus. J Mol Evol 41:104–112
Bidwell CA, Kroll KJ, Severud E, Doroshov SI, Carlson DM (1991) Identification and preliminary characterization of white sturgeon (Acipenser transmontanus) vitellogenin mRNA. Gen Comp Endocrinol 83:415–424
Breton TS, Anderson JL, Goetz FW, Berlinsky DL (2012) Identification of ovarian gene expression patterns during vitellogenesis in Atlantic cod (Gadus morhua). Gen Comp Endocrinol 179:296–304
Bruch RM, Dick TA, Choudhury A (2001) A field guide for the identification of stages of gonad development in lake sturgeon (Acipenser fulvescens: Rafinesque): with note on lake sturgeon reproductive biology and management implications. Sturgeon for Tomorrow, Fond du Lac, 38
Carnevali O, Cionna C, Tosti L, Lubzens E, Maradonna F (2006) Role of cathepsins in ovarian follicle growth and maturation. Gen Comp Endocrinol 146:195–203
Chapman FA, Park C (2005) Comparison of sutures used for wound closure in sturgeon following a gonad biopsy. N Am J Aquac 67:98–101
Chatterjee C, Sparks DL (2011) Hepatic lipase, high density lipoproteins, and hypertriglyceridemia. Am J Pathol 178:1429–1433
Chebanov M, Galich EV (2011) Sturgeon hatchery manual. FAO Fisheries and Aquaculture Technical Paper, 338
Dettlaff TA, Ginsburg AS, Schmalhausen OI (1993) Sturgeon fishes: developmental biology and aquaculture. Springer, New York
Ding X, Nagaraju GPC, Novotney D, Lovett DL, Borst DW (2010) Yolk protein expression in the green crab, Carcinus maenas. Aquaculture 298:325–331
Doroshov SI, Moberg GP, Van Eenennaam JP (1997) Observations on the reproductive cycle of cultured white sturgeon, Acipenser transmontanus. Environ Biol Fish 48:265–278
Doumas BT, Bayse DD, Carter RJ, Peters TJR, Schaffer RA (1981) Candidate reference method for determination of total protein in serum. I. Development and validation. Clin Chem 10:42–50
Falahatkar B, Poursaeid S, Shakoorian M, Barton B (2009) Responses to handling and confinement stressors in juvenile great sturgeon Huso huso. J Fish Biol 75:784–796
Falahatkar B, Tolouei MH, Falahatkar S, Abbasalizadeh A (2011) Laparoscopy, a minimally-invasive technique for sex identification in cultured great sturgeon Huso huso. Aquaculture 321:273–279
Falahatkar B, Akhavan SR, Tolouei Gilani MH, Abbasalizadeh A (2013) Sex identification and sexual maturity stages in farmed great sturgeon, Huso huso L. through biopsy. Iran J Vet Res 14:133–139
Folmart LC, Moody T, Bonomelli S, Gibson J (1992) Annual cycle of blood chemistry parameters in striped mullet (Mugil cephalus L.) and pinfish (Lagodon rhomboids L.) from the Gulf of Mexico. J Fish Biol 41:999–1011
Friedewald WT, Levy RI, Fredrickson DS (1972) Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin Chem 18:499–502
Gharaei A, Ghaffari M, Keyvanshokooh S, Akrami R (2011) Changes in metabolic enzymes, cortisol and glucose concentrations of Beluga (Huso huso) exposed to dietary methylmercury. Fish Physiol Biochem 37:485–493
Ghiasi S, Falahatkar B, Dabrowski K, Arslan M (2014) Effect of thiamine injection on growth performance, hematology and germinal vesicle migration in sterlet sturgeon Acipenser ruthenus L. Aquac Int 22:1563–1576
Gibbons GF, Wiggins D (1995) Intracellular triacylglycerol lipase:its role in the assembly of hepatic very-low-density lipoprotein (VLDL). Adv Enzyme Regul 35:179–198
Gindler ME, King JD (1972) Rapid colorometric determination of calcium in biological fluids with methyl thymol blue. Am J Clin Pathol 58:376–382
Henderson RI, Tocher DR (1987) The lipid composition and biochemistry of freshwater fish. Prog Lipid Res 26:281–347
Henry RJ, Cannon DC, Winkelman JW (1974) Clinical chemistry: principles and techniques, 2nd edn. Harperand Row Publisher, Hagerstown, pp 287–341
Holčik J (1989) The freshwater fishes of Europe, vol. 1 part II, general introduction to fishes acipenseriformes, AULA-Verlag, Wiesbaden
Ibanez AJ, Peinado-Onsurbe J, Sanchez E, Cerda-Reverter JM, Prat F (2008) Lipoprotein lipase (LPL) is highly expressed and active in the ovary of European sea bass (Dicentrarchus labrax L.), during gonadal development. Comp Biochem Physiol A: Mol Integr Physiol 150:347–354
Iijima N, Ueki T, Yoshitake S, Kayama M (1990) Isolation and characterization of carp plasma lipoproteins. Nippon Suisan Gakkaishi 56:1113–1122
Jonas A, Phillips MC (2008) Lipoproteinstructure. In: Vance DE, Vance JE (eds) Biochemistry of lipids, lipoproteins and membranes, 5th edn. Elsevier, Edmonton
Kang BJ, Nanri T, Lee JM, Saito H, Han CH, Hatakeyama M, Saigusa M (2008) Vitellogenesis in both sexes of gonochoristic mud shrimp, Upogebia major (Crustacea): analyses of vitellogenin gene expression and vitellogeninprocessing. Comp Biochem Physiol B: Biochem Mol Biol 149:589–598
Kong HJ, Kim JL, Moon JY, Kim WJ, Kim HS, Park JY, Cho HK, An CM (2014) Characterization, expression profile, and promoter analysis of the Rhodeus uyekii vitellogenin Ao1 gene. Int J Mol Sci 15:18804–18818
Kroll KJ (1990) Preliminary characterization of vitellogenin and yolk proteins of the white Sturgeon (Acipenser transmontanus). Dissertation, University of California, Davis
Kumar S, Sahu NP, Pal AK, Choudhury D, Yengkokpam S, Mukherjee SC (2005) Efffect of dietary carbohydrate on haematology, respiratory burst activity and histological changes in L. rohita juveniles. Fish Shellfish Immunol 19:331–334
Kwon JY, Prat F, Randall C, Tyler CR (2001) Molecular characterization of putative yolk processing enzymes and their expression during oogenesis and embryogenesis in rainbow trout (Oncorhynchus mykiss). Biol Reprod 65:1701–1709
Leger C, Fremont L, Boudon M (1981) Fatty acid composition of lipids in the trout. I. Influence of dietary fatty acids on the triglyceride fatty acid desaturation in serum, adipose tissue, liver, white and red muscle. Comp Biochem Physiol 69B:99–105
Linares-Casenave J, Van Eenennaam JP, Doroshov SI (2002) Ultrastructural and histological observations on temperature-induced follicular ovarian atresia in the white sturgeon. J Appl Ichthyol 18:382–390
Linares-Casenave J, Kroll KJ, Van Eenennaam JP, Doroshov SI (2003) Effect of ovarian stage on plasma vitellogenin and calcium in cultured white sturgeon. Aquaculture 221:645–656
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCt method. Methods 25:402–408
Lubzens E, Young G, Bobe J, Cerda J (2010) Oogenesis in teleosts: how fish eggs are formed. Gen Comp Endocrinol 165:367–389
Lund ED, Sullivan CV, Place AR (2000) Annual cycle of plasma lipids in captive reared striped bass: effects of environmental conditions and reproductive cycle. Fish Physiol Biochem 22:263–275
Ma J, Zhang T, Zhuang P, Yan SW, Zhang LZ, Tian MP, Gao LJ (2011) The role of lipase in blood lipoprotein metabolism and accumulation of lipids in oocytes of the Siberian sturgeon Acipenser baerii during maturation. J Appl Ichthyol 27:246–250
Mead JR, Irvine SA, Ramji DP (2002) Lipoprotein lipase: structure, function, regulation, and role in disease. J Mol Med 80:753–769
Mekki K, Prost J, Bouchenak M, Remaoun M, Belleville J (2003) Plasma lipoprotein lipase, hepatic lipase activities, VLDL, LDL compositions at different times of hemodialysis. Atherosclerosis 169:269–277
Moberg GP, Doroshov SI, Chapman FA, Kroll KJ, Van Eenennaam J, Watson JG (1991) Effects of various hormone implants on vitellogenin synthesis and ovarian development in cultured white sturgeon, Acipenser transmontanus. In: Bordeaux G, Williot P (ed) Proceedings of the first international symposium on sturgeon. France, October 3–6, 1989, pp 389–399
Mommsen TP, Walsh PL (1988) Vitellogenesis and oocyte assembly. In: Hoar WS, Randall DJ (eds) Fish physiology, vol XIA. Academic Press, New York, pp 347–406
Patino R, Sullivan CV (2002) Ovarian follicle growth, maturation, and ovulation in teleost fish. Fish Physiol Biochem 26:57–70
Pelissero C, Cuisset B, Le Menn F (1989) The influence of sex steroid in commercial fish meals and fish diets on plasma concentration of estrogens and vit1llogenin in cultured Siberian sturgeon Acipenser baeri. Aquat Living Resour 2:161–168
Rick W (1990) Klinische chemie und mikroskopie, 6th edn. Springer, Berlin, p 294
Rifai N, Bachorik PS, Albers JJ (1999) Lipids, lipoproteins and apolipoproteins. In: Burtis CA, Ashwood ER (eds) Tietz textbook of clinical chemistry, 3rd edn. Saunders Company, Philadelphia, pp 809–861
Roubal W, Lomax DP, Willis ML, Johnson LL (1997) Purification and partial characterization of English sole (Pleuronectes vetukus) vitellogenin. Comp Biochem Physiol 11B:613–622
Santamarina-Fojo S, Haudenschild C, Amar M (1998) The role of hepatic lipase in lipoprotein metabolism and atherosclerosis. Curr Opin Lipidol 9:211–219
Schmid T, Gonzalez-Valero J, Rufli H, Dietrich DR (2002) Determination of vitellogenin kinetics in male fathead minnows (Pimephales promelas). Toxicol Lett 131:65–74
Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C (T) method. Nat Protoc 3:1101–1108
Sharpe RL, MacLatchy DL (2007) Lipid dynamics in goldfish (Carassius auratus) during a period of gonadal recrudescence: effects of β-sitosterol and 17β-estradiol exposure. Comp Biochem Physiol 145:507–517
Singh S, Srivastav AK (1990) Changes in the serum calcium and phosphate levels in relation to the annual reproductive cycle of the freshwater catfish, Heteropneustes fossilis. Bol Physiol Anim 14:81–86
Srivastav SK, Srivastav AK (1998) Annual changes in serum calcium and inorganic phosphate levels and correlation with gonadal status of a freshwater murrel, Channa punctatus (Bloch). Braz J Med Biol Res 31:1069–1073
Tyler CR, Sumpter JP (1996) Oocyte growth and development in teleost. Rev Fish Biol Fish 6:287–318
Van Eenennaam JP, Doroshov SI, Moberg GP, Watson JD, Moore DS, Linares J (1996) Reproductive conditions of Atlantic sturgeon (Acipenser oxyrinchus) in the Hudson, River. Estuaries 19:769–777
Wallace RA (1985) Vitellogenesis and oocyte growth in nonmammalian vertebrales. In: Browder LW (ed) Developmental biology, vol. I: oogenesis. Plenum Press, New York, p 127
Wallaert C, Babin PJ (1994) Age-related, sex-related, and seasonal changes of plasma lipoprotein concentrations in trout. J Lipid Res 35:1619–1633
Wang R, Gao Y, Zhang L, Zhang Y, Fang Z, He J, Zhang W, Ma G (2010) Cloning, expression, and induction by 17-beta estradiol (E2) of a vitellogenin gene in the white cloud mountain minnow Tanichthys albonubes. Fish Physiol Biochem 36:157–164
Wiegand M (1996) Composition, accumulation and utilization of yolk lipids in teleost fish. Rev Fish Biol Fish 6:259–286
Williot P, Brun R (1998) Ovarian development and cycles in cultured Siberian sturgeon, Acipenser baeri. Aquat Living Resour 11:111–118
Zhang Z, Hu J, Fenjin W, An W, Jin F, An L, Tao S, Chen J (2005) Induction of vitellogenin mRNA in juvenile Chinese sturgeon (Acipenser sinensis) treated with 17β-estradiol and 4-nonylphenol. Environ Toxicol Chem 24:1944–1950
Zhang LZ, Zhang T, Zhuang P, Zhao F, Wang B, Feng GP, Song C, Wang Y, Xu SJ (2014) Discriminant analysis of blood biochemical parameters at different developmental gonad stages and gender identification for controlled breeding of Amur sturgeon (Acipenser schrenckii, Brandt, 1869). J Appl Ichthyol 30:1207–1211
Zmora N, Trant J, Chan SM, Chung JS (2007) Vitellogenin and its messenger RNA during ovarian devel-opment in the female blue crab, Callinectes sapidus: gene expression, synthesis, transport, and cleavage. Biol Reprod 77:138–146
Acknowledgments
The authors gratefully acknowledge of the Shahid Dr. Beheshti Sturgeon Fish Propagating and Rearing Complex for supplying the fish and also Institute of Biotechnology and Bioengineering Isfahan University of Technology providing the facilities for molecular experiments.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Akhavan, S.R., Salati, A.P., Falahatkar, B. et al. Changes of vitellogenin and Lipase in captive Sterlet sturgeon Acipenser ruthenus females during previtellogenesis to early atresia. Fish Physiol Biochem 42, 967–978 (2016). https://doi.org/10.1007/s10695-015-0189-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10695-015-0189-8