Differential processing of yolk proteins during oocyte hydration in marine fishes (Labridae) that spawn benthic and pelagic eggs

Finn, Roderick Nigel; Wamboldt, Melissa; Fyhn, Hans Jørgen

doi:10.3354/meps237217

Cited by 37 publications

(29 citation statements)

References 47 publications

(45 reference statements)

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“…Increasing the intracellular volume through the influx of water will thus achieve buoyancy in proportion to 3/r, where r is the radius of the egg. These proposals are supported by the observation that a large halibut OV egg swells only ;4-fold, while a small Labrid pelagic egg (0.86 mm) swells 6.5-8.4-fold compared to the PH ooc [1,2]. In contrast to these type I eggs, the presence of oil globules in type II eggs contributes to buoyancy, and therefore the degree of proteolysis may be lower in such eggs [57,58].…”

Section: Yolk Proteolysismentioning

confidence: 90%

“…The degree of proteolysis has been shown to be related to the type of egg spawned, e.g., benthic or pelagic, and also to the differential expression of the vtg genes [15,21,23]. In benthic eggs, the yolk proteins are either not processed or are partially cleaved and hydrolyzed, while in pelagic eggs, the yolk proteins are not only cleaved but undergo extensive proteolysis, resulting in the buildup of the FAA pool [1,2]. The FAA are the major osmolytes that drive the maturational influx of water via specific aquaporins [4,5], thereby providing the early embryo of marine teleosts with a vital water reservoir before a drinking mechanism is developed [1].…”

Section: Introductionmentioning

confidence: 99%

“…We have argued that it is a vital reproductive process in marine teleosts in that it preadapts the eggs to the hyperosmotic spawning environment [1][2][3]. In response to external and maternal signals that involve the brain-pitutary-gonad axis, a suite of co-ordinated events are set in motion, leading to the osmotic flow of water from the maternal plasma to the oocyte via specialized aquaporins that are temporally inserted in the oocyte plasma membrane during this period [4,5].…”

Section: Introductionmentioning

confidence: 99%

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The Maturational Disassembly and Differential Proteolysis of Paralogous Vitellogenins in a Marine Pelagophil Teleost: A Conserved Mechanism of Oocyte Hydration1

Finn

2007

Biology of Reproduction

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A structural analysis of the differential proteolysis of vitellogenin (Vtg)-derived yolk proteins in the maturing oocytes of a marine teleost that spawns very large pelagic eggs is presented. Two full-length hepatic cDNAs (hhvtgAa and hhvtgAb) encoding paralogous vitellogenins (HhvtgAa and HhvtgAb) were cloned from nonestrogenized Atlantic halibut, and the N-termini of their subdomain structures were mapped to the oocyte and egg yolk proteins (Yps). The maturational oocyte Yp degradation products were further mapped to the free amino acid (FAA) pool in the ovulated egg. The deduced amino acid sequences conformed to the linear NH(2)-(LvH-Pv-LvL-beta'-CT)-COO(-) structure of complete teleost Vtgs. However, the Yps did not match the expected cleavage products of complete Vtgs. Specifically, the phosvitin subdomain of the HhvtgAa paralogue remains covalently attached to the lipovitellin light chain, while the phosvitin subdomain of the HhvtgAb paralogue remains covalently attached to a C-terminal fragment of the lipovitellin heavy chain (LvH). During oocyte hydration, the LvH of the HhvtgAa paralogue is disassembled and extensively degraded to FAA. In the HhvtgAb paralogue, the LvH is nicked in the C-sheet in a manner similar to that seen in lamprey and other teleosts. A small part of the C-terminal end of the LvH-Ab undergoes proteolysis to FAA, together with the phosvitin, beta' component, and much ( approximately 65%) of the lipovitellin light chain (LvL-Ab). The independently measured FAA pool in the ovulated egg corroborates that calculated from differential proteolysis of the Yps. Based on the 3:1 (HhvtgAb:HhvtgAa) Yp expression ratio, each paralogue contributes approximately equal amounts of FAA to the organic osmolyte pool of the hydrating oocyte during maturation.

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Section: Yolk Proteolysismentioning

confidence: 90%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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The Maturational Disassembly and Differential Proteolysis of Paralogous Vitellogenins in a Marine Pelagophil Teleost: A Conserved Mechanism of Oocyte Hydration1

Finn

2007

Biology of Reproduction

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“…In some freshwater species, such as zebrafish, electrophoretic band-shifts of the LvH occurs during oocyte maturation due to nicking [82], but no proteolysis, and no buildup of FAA occurs (Finn, unpublished data), which would be osmotically disadvantageous to the freshwater embryo. During oocyte maturation in marine benthophils the yolk proteins are either not processed, or are partially cleaved and hydrolyzed with the release of a small pool of FAA [69], [73], while in marine pelagophils, the yolk proteins are not only cleaved but undergo extensive differential proteolysis of particularly one of the LvH domains resulting in the buildup of the large pool of FAA. The transient increase in osmolarity during oocyte maturation [57] causes water influx via specialized aquaporins that are temporally inserted in the plasma membrane during this period [83], [84].…”

Section: Introductionmentioning

confidence: 99%

Vertebrate Vitellogenin Gene Duplication in Relation to the “3R Hypothesis”: Correlation to the Pelagic Egg and the Oceanic Radiation of Teleosts

2007

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The spiny ray-finned teleost fishes (Acanthomorpha) are the most successful group of vertebrates in terms of species diversity. Their meteoric radiation and speciation in the oceans during the late Cretaceous and Eocene epoch is unprecedented in vertebrate history, occurring in one third of the time for similar diversity to appear in the birds and mammals. The success of marine teleosts is even more remarkable considering their long freshwater ancestry, since it implies solving major physiological challenges when freely broadcasting their eggs in the hyper-osmotic conditions of seawater. Most extant marine teleosts spawn highly hydrated pelagic eggs, due to differential proteolysis of vitellogenin (Vtg)-derived yolk proteins. The maturational degradation of Vtg involves depolymerization of mainly the lipovitellin heavy chain (LvH) of one form of Vtg to generate a large pool of free amino acids (FAA 150–200 mM). This organic osmolyte pool drives hydration of the ooctye while still protected within the maternal ovary. In the present contribution, we have used Bayesian analysis to examine the evolution of vertebrate Vtg genes in relation to the “3R hypothesis” of whole genome duplication (WGD) and the functional end points of LvH degradation during oocyte maturation. We find that teleost Vtgs have experienced a post-R3 lineage-specific gene duplication to form paralogous clusters that correlate to the pelagic and benthic character of the eggs. Neo-functionalization allowed one paralogue to be proteolyzed to FAA driving hydration of the maturing oocytes, which pre-adapts them to the marine environment and causes them to float. The timing of these events matches the appearance of the Acanthomorpha in the fossil record. We discuss the significance of these adaptations in relation to ancestral physiological features, and propose that the neo-functionalization of duplicated Vtg genes was a key event in the evolution and success of the teleosts in the oceanic environment.

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“…Oocyte swelling due to water entry may reach about two-to fivefold the initial volume (Greeley et al, 1986;Selman and Wallace, 1983;Watanabe and Kuo, 1986). This results in the adjustment of the buoyancy of ovulated eggs either to pelagic or to benthic characteristics, depending on the species (Finn et al, 2002b;Finn et al, 2002a;Fyhn et al, 1999). Hydration appears to be induced by the combination of two different biological processes leading to a transient increase of yolk osmolarity.…”

Section: Introductionmentioning

confidence: 99%

Hydration of rainbow trout oocyte during meiotic maturation andin vitroregulation by 17,20β-dihydroxy-4-pregnen-3-one and cortisol

Milla¹,

Jalabert²,

Rime³

et al. 2006

Journal of Experimental Biology

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Although oocytes of many teleost fish, especially marine species, are subjected to a hydration process during meiotic maturation, which leads to an important volume increase, no noticeable hydration of the preovulatory oocyte has ever been reported in rainbow trout (Oncorhynchus mykiss). In the present study, oocyte water content and dry mass were monitored using consecutive samples taken in vivo from the same female rainbow trout, from 4-5·days prior to ovulation to up to 7·days postovulation. In addition, yolk protein electrophoretic patterns were compared between oocytes sampled prior to germinal vesicle breakdown (GVBD) and unfertilized eggs. Furthermore, the effect of the maturation-inducing steroid (17,20␤ ␤-dihydroxy-4-pregnen-3-one, 17,20␤ ␤-P), cortisol and 11-deoxycorticosterone (DOC) on oocyte dry and wet masses, as well as GVBD occurrence was assessed in vitro. Finally, mRNA expression profiles of glucocorticoid and mineralocorticoid receptors as well as 11␤ ␤-hydroxysteroid dehydrogenase (11␤ ␤-HSD) were monitored in the periovulatory ovary by real-time PCR.Both in vivo and in vitro data showed, for the first time in rainbow trout, that a significant oocyte hydration occurs during oocyte maturation. In addition, an intra-oocyte dry matter increase was reported in vivo during the periovulatory period. However, yolk protein migration patterns were similar in preGVBD oocytes and unfertilized eggs, suggesting that no or little yolk proteolysis occurs during oocyte maturation. We also showed that oocyte hydration can be induced in vitro by 17,20␤ ␤-P and cortisol but not by DOC. In contrast, GVBD was only observed after 17,20␤ ␤-P stimulation. Finally, real-time PCR analysis showed an up-regulation of 11␤ ␤-HSD and glucocorticoid receptor 2 transcripts in the ovary at the time of oocyte maturation. Together, these results suggest that cortisol could participate in the control of oocyte hydration and possibly in other periovulatory ovarian functions.

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Differential processing of yolk proteins during oocyte hydration in marine fishes (Labridae) that spawn benthic and pelagic eggs

Cited by 37 publications

References 47 publications

The Maturational Disassembly and Differential Proteolysis of Paralogous Vitellogenins in a Marine Pelagophil Teleost: A Conserved Mechanism of Oocyte Hydration1

The Maturational Disassembly and Differential Proteolysis of Paralogous Vitellogenins in a Marine Pelagophil Teleost: A Conserved Mechanism of Oocyte Hydration1

Vertebrate Vitellogenin Gene Duplication in Relation to the “3R Hypothesis”: Correlation to the Pelagic Egg and the Oceanic Radiation of Teleosts

Hydration of rainbow trout oocyte during meiotic maturation andin vitroregulation by 17,20β-dihydroxy-4-pregnen-3-one and cortisol

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