Structural requirements for species-specific induction of the sperm acrosome reaction by sea urchin egg sulfated fucan

Hirohashi, Noritaka; Vilela-Silva, Ana-Cristina E.S.; Mourāo, Paulo A.S.; Vacquier, Victor D.

doi:10.1016/s0006-291x(02)02441-5

Cited by 36 publications

(18 citation statements)

References 16 publications

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“…The fact that the sulfated fucans are species-specific AR inducers was confirmed as the study was extended to the species Strongylocentrotus franciscanus and Strongylocentrotus purpuratus, both from the eastern north Pacific (Vilela-Silva et al, 1999;Hirohashi et al, 2002a). These species contain 3-linked fucans, which differ in the proportions of 2-and 4-sulfation.…”

Section: Unique Sulfated Polysaccharides In Sea Urchin Egg Jellymentioning

confidence: 69%

“…Thus, a 2-sulfated, 4-linked fucan is inactive on S. franciscanus sperm, which recognize the homologous 2-sulfated, but 3-linked fucan (Hirohashi et al, 2002a). Various 3-linked fucans, with variable sulfation at 2-and/or 4 positions are inactive on S. droebachiensis, which has a 4-linked fucan (Fig.…”

Section: Unique Sulfated Polysaccharides In Sea Urchin Egg Jellymentioning

confidence: 97%

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The structure of sulfated polysaccharides ensures a carbohydrate-based mechanism for species recognition during sea urchin fertilization

Vilela-Silva

Hirohashi²,

Mourāo

2008

Int. J. Dev. Biol.

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The evolution of barriers to inter-specific hybridization is a crucial step in the fertilization of free spawning marine invertebrates. In sea urchins, molecular recognition between sperm and egg ensures species recognition. Here we review the sulfated polysaccharide-based mechanism of sperm-egg recognition in this model organism. The jelly surrounding sea urchin eggs is not a simple accessory structure; it is molecularly complex and intimately involved in gamete recognition. It contains sulfated polysaccharides, sialoglycans and peptides. The sulfated polysaccharides have unique structures, composed of repetitive units of α-L-fucose or α-Lgalactose, which differ among species in the sulfation pattern and/or the position of the glycosidic linkage. The egg jelly sulfated polysaccharides show species-specificity in inducing the sperm acrosome reaction, which is regulated by the structure of the saccharide chain and its sulfation pattern. Other components of the egg jelly do not possess acrosome reaction inducing activity, but sialoglycans act in synergy with the sulfated polysaccharide, potentiating its activity. The system we describe establishes a new view of cell-cell interaction in the sea urchin model system. Here, structural changes in egg jelly polysaccharides modulate cell-cell recognition and speciesspecificity leading to exocytosis of the acrosome. Therefore, sulfated polysaccharides, in addition to their known functions as growth factors, coagulation factors and selectin binding partners, also function in fertilization. The differentiation of these molecules may play a role in sea urchin speciation.

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Section: Unique Sulfated Polysaccharides In Sea Urchin Egg Jellymentioning

confidence: 69%

Section: Unique Sulfated Polysaccharides In Sea Urchin Egg Jellymentioning

confidence: 97%

The structure of sulfated polysaccharides ensures a carbohydrate-based mechanism for species recognition during sea urchin fertilization

Vilela-Silva

Hirohashi²,

Mourāo

2008

Int. J. Dev. Biol.

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“…A prerequisite for the entry of the sperm into eggs is the acrosome reaction because the egg plasma membrane can only fuse with the newly formed membrane of the acrosomal process. In sea urchin, sulfated fucoserich compounds in the jelly coat of the egg provide speciesspecificity in inducing the acrosome reaction (Hirohashi et al, 2002). Within 2-4 sec following the attachment of the fertilizing spermatozoon to the vitelline coat, a step-like depolarization occurs across the egg plasma membrane, probably due to a factor released from the acrosome in the proximity of the egg plasma membrane (Longo et al, 1986).…”

Section: Sperm-egg Interaction At Fertilizationmentioning

confidence: 99%

The role of the actin cytoskeleton in calcium signaling in starfish oocytes

Santella

Puppo²,

Chun³

2008

Int. J. Dev. Biol.

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Ca 2+ is the most universal second messenger in cells from the very first moment of fertilization. In all animal species, fertilized eggs exhibit massive mobilization of intracellular Ca 2+ to orchestrate the initial events of development. Echinoderm eggs have been an excellent model system for studying fertilization and the cell cycle due to their large size and abundance. In preparation for fertilization, the cell cycle-arrested oocytes must undergo meiotic maturation. Studies of starfish oocytes have shown that Ca 2+ signaling is intimately involved in this process. Our knowledge of the molecular mechanism of meiotic maturation and fertilization has expanded greatly in the past two decades due to the discovery of cell cycle-related kinases and Ca 2+ -mobilizing second messengers. However, the molecular details of their actions await elucidation of other cellular elements that assist in the creation and transduction of Ca 2+ signals. In this regard, the actin cytoskeleton, the receptors for second messengers and the Ca 2+ -binding proteins also require more attention. This article reviews the physiological significance and the mechanism of intracellular Ca 2+ mobilization in starfish oocytes during maturation and fertilization. KEY WORDS: cell activation, sperm-egg interaction, meiosis, germinal vesicle, cyclic ADP ribose, NAADP Starfish oocytes and maturation-promoting factorStarfish oocytes have contributed greatly to our understanding of the molecular mechanisms controlling the cell cycle (maturation) and fertilization. During oogenesis, the oocytes undergo cell growth and differentiation bringing them to the end of the first prophase of meiosis where they remain synchronously arrested until spawning (Fig. 1). At this stage of maturation, the oocytes are characterized by a very large nucleus (approximately 60 µm in diameter) termed the germinal vesicle (GV) (Fig. 2). The starfish oocyte has several advantages as an experimental model system. First, the cell is large and nearly transparent, making it suitable for imaging experiments after microinjection of fluorescent markers. Second, maturation (or meiosis re-initiation) can be induced in vivo and in vitro by the hormone 1-methyladenine (1-MA), rendering the oocytes successfully fertilizable (Kanatani et al., 1969;Meijer and Guerrier, 1984). The first visible sign of oocyte maturation is the germinal vesicle breakdown (GVBD) in which the large nucleus breaks down to release its nucleoplasm into the cytoplasm 20-30 minutes after the application of the hormone. This is how the starfish oocyte is conspicuously different from sea urchin eggs, which are already mature at the time of spawning. In sea urchins, the haploid egg pronucleus has a Int. J. Dev. Biol. 52: 571-584 (2008) doi: 10.1387/ijdb.072560ls Abbreviations used in this paper: cADPr, cyclic-ADPribose; CaMKII, calmodulin dependent kinase II; CICR, calcium induced calcium release; GV, germinal vesicle; GVBD, germinal vesicle breakdown; InsP3, inositol 1,4,5-trisphosphate; LAT-A, latrunculin-...

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“…The fact that the sulfated fucans are species-specific inducers of the acrosome reaction in sea urchins was confirmed when the study was extended to the species Strongylocentrotus franciscanus and S. purpuratus, both from the North Pacific Ocean (41,49). These species contain 3-linked fucans, which differ in the proportions of 2-and 4-sulfation.…”

Section: Unique Sulfated Fucans In Echinodermsmentioning

confidence: 79%

A carbohydrate-based mechanism of species recognition in sea urchin fertilization

Mourāo

2007

Braz J Med Biol Res

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In the present review, we describe a systematic study of the sulfated polysaccharides from marine invertebrates, which led to the discovery of a carbohydrate-based mechanism of sperm-egg recognition during sea urchin fertilization. We have described unique polymers present in these organisms, especially sulfated fucose-rich compounds found in the egg jelly coat of sea urchins. The polysaccharides have simple, linear structures consisting of repeating units of oligosaccharides. They differ among the various species of sea urchins in specific patterns of sulfation and/or position of the glycosidic linkage within their repeating units. These polysaccharides show species specificity in inducing the acrosome reaction in sea urchin sperm, providing a clear-cut example of a signal transduction event regulated by sulfated polysaccharides. This distinct carbohydrate-mediated mechanism of sperm-egg recognition coexists with the bindin-protein system. Possibly, the genes involved in the biosynthesis of these sulfated fucans did not evolve in concordance with evolutionary distance but underwent a dramatic change near the tip of the Strongylocentrotid tree. Overall, we established a direct causal link between the molecular structure of a sulfated polysaccharide and a cellular physiological event -the induction of the sperm acrosome reaction in sea urchins. Small structural changes modulate an entire system of sperm-egg recognition and species-specific fertilization in sea urchins. We demonstrated that sulfated polysaccharides -in addition to their known function in cell proliferation, development, coagulation, and viral infectionmediate fertilization, and respond to evolutionary mechanisms that lead to species diversity.

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Structural requirements for species-specific induction of the sperm acrosome reaction by sea urchin egg sulfated fucan

Cited by 36 publications

References 16 publications

The structure of sulfated polysaccharides ensures a carbohydrate-based mechanism for species recognition during sea urchin fertilization

The structure of sulfated polysaccharides ensures a carbohydrate-based mechanism for species recognition during sea urchin fertilization

The role of the actin cytoskeleton in calcium signaling in starfish oocytes

A carbohydrate-based mechanism of species recognition in sea urchin fertilization

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