Assembly of the fertilization membrane of the sea urchin: Isolation of a divalent cation-dependent intermediate and its crosslinking in vitro

Kay, Erica S.; Eddy, E. M.; Shapiro, Bennett M.

doi:10.1016/0092-8674(82)90448-2

Cited by 46 publications

(26 citation statements)

References 30 publications

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…What distinguishes yeast dityrosine is its unique pathway of synthesis. In the sea urchin egg, for instance, dityrosine is formed in a one-step reaction directly in the fertilization membrane (21). In contrast, dityrosine synthesis in S. cerevisiae is far more complex and involves several consecutive steps (6).…”

Section: Discussionmentioning

confidence: 99%

Dtr1p, a Multidrug Resistance Transporter of the Major Facilitator Superfamily, Plays an Essential Role in Spore Wall Maturation in Saccharomyces cerevisiae

et al. 2002

View full text Add to dashboard Cite

The de novo formation of multilayered spore walls inside a diploid mother cell is a major landmark of sporulation in the yeast Saccharomyces cerevisiae. Synthesis of the dityrosine-rich outer spore wall takes place toward the end of this process. Bisformyl dityrosine, the major building block of the spore surface, is synthesized in a multistep process in the cytoplasm of the prospores, transported to the maturing wall, and polymerized into a highly cross-linked macromolecule on the spore surface. Here we present evidence that the sporulation-specific protein Dtr1p (encoded by YBR180w) plays an important role in spore wall synthesis by facilitating the translocation of bisformyl dityrosine through the prospore membrane. DTR1 was identified in a genome-wide screen for spore wall mutants. The null mutant accumulates unusually large amounts of bisformyl dityrosine in the cytoplasm and fails to efficiently incorporate this precursor into the spore surface. As a result, many mutant spores have aberrant surface structures. Dtr1p, a member of the poorly characterized DHA12 (drug:H ؉ antiporter with 12 predicted membrane spans) family, is localized in the prospore membrane throughout spore maturation. Transport by Dtr1p may not be restricted to its natural substrate, bisformyl dityrosine. When expressed in vegetative cells, Dtr1p renders these cells slightly more resistant against unrelated toxic compounds, such as antimalarial drugs and food-grade organic acid preservatives. Dtr1p is the first multidrug resistance protein of the major facilitator superfamily with an assigned physiological role in the yeast cell.Diploid a/␣ cells of the budding yeast Saccharomyces cerevisiae undergo a specialized developmental program termed sporulation when transferred to a nitrogen-free medium containing potassium acetate as nonfermentable carbon source. The final product of sporulation is an ascus that consists of four haploid spores surrounded by the ascus wall, the former vegetative cell wall (for a review, see reference 27). Spores are protected from adverse environmental conditions by the spore wall. Especially the surface layers contribute both to the spores' mechanical rigidity and their resistance against chemical and enzymatic attack (3). Spore wall synthesis begins with the formation of the prospore membrane, a bilayered electrondense structure that starts to form during the second meiotic division on the cytoplasmic side of each of the four spindle pole bodies by fusion of secretory vesicles (9, 13, 23, 31-33). As meiosis progresses, the prospore membrane extends along the outer surface of the nuclear envelope. Septins, among them the sporulation-specific proteins Spr3p and Spr28p, localize at the leading tip of the prospore membrane under control of the Gip1p-Glc7p phosphatase complex and might be involved in its extension and directed growth (14,16,44). Other proteins localized to the growing prospore membrane are SspIp, Ady3p, and Don1p, which form the leading edge protein coat (23,33) and presumably Sps2p (11,38), but th...

show abstract

Section: Discussionmentioning

confidence: 99%

Dtr1p, a Multidrug Resistance Transporter of the Major Facilitator Superfamily, Plays an Essential Role in Spore Wall Maturation in Saccharomyces cerevisiae

et al. 2002

View full text Add to dashboard Cite

show abstract

“…Ovoperoxidase catalyzes protein crosslinking most efficiently after assembly (31), suggesting that proteoliaisin juxtaposes ovoperoxidase and its substrates appropriately for the hardening reaction to occur. Thus, the assembly of an uncrosslinked soft fertilization envelope that is dependent upon the presence of divalent cations for its stability (7,9,29) is a prerequisite for the hardening reaction. A limited subset of fertilization envelope components, in addition to proteoliaisin and the vitelline layer (41), serves as the target for cosslinking in vivo (29,31).…”

Section: Envelope Hardeningmentioning

confidence: 99%

“…Its high glycine content suggests proteoliaisin to be a flexible rod. Although proteoliaisin is a substrate for ovoperoxidasecatalyzed dityrosine formation in vivo (29,31), it contains relatively few aromatic amino acids (ca. 50 tyrosines/ molecule).…”

Section: Proteoliaisinmentioning

confidence: 99%

“…It uses H202 formed in a CN --insensitive respiratory burst at fertilization (22) to catalyze the formation of dityrosine crosslinks between a subset of adjacent polypeptides in the assembled fertilization envelope (15,21,24,29,31). Purified ovoperoxidase is a 70,000 Mr hemeglycoprotein that is similar but not identical in catalytic and spectral properties to lactoperoxidase (15).…”

Section: Ovoperoxidasementioning

confidence: 99%

“…Starting at the site of sperm-egg fusion the vitelline layer elevates from the egg surface and undergoes a structural rearrangement such that its fibrous network is converted into a trilaminar extracellular matrix (1 2, 13, 26). Secreted proteins effect this change by assembling upon the vitelline layer scaffold through specific ionic interactions (7,9,29,43). Finally, a secreted ovoperoxidase uses H202 produced by the egg to catalyze the covalent crosslinking of a subset of proteins to give rise to the final structure (15,21,22,24,29,31).…”

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

Insights into the Molecular Mechanisms Involved in Sea Urchin Fertilization Envelope Assembly

Somers

Shapiro

1989

Dev Growth Differ

Self Cite

View full text Add to dashboard Cite

Sea urchin fertilization envelope assembly provides an ideal model system for investigating the production and modification of an extracellular matrix. The contents of secretory vesicles and the egg glycocalyx mix to initiate assembly. Limited proteolysis and covalent crosslinking by a transglutaminase act as early events to modify the nascent envelope. A subset of secreted proteins binds to this matrix through ionic interactions that require divalent cations. For example, one secreted protein, proteoliaisin, is responsible for attaching ovoperoxidase to the envelope. Ovoperoxidase hardens the envelope by using hydrogen peroxide, produced by the egg during the respiratory burst, to form dityrosine crosslinks between a subset of fertilization envelope proteins. Numerous spatial and temporal regulatory mechanisms exist to ensure that proper assembly occurs in an environment isolated from the normal cytosolic regulatory machinery.

show abstract

Presence of a proteinase inhibitor in the vitelline envelope and its role in eggs of the fishTribolodon hakonensis

Kudo

1998

J. Exp. Zool.

View full text Add to dashboard Cite

Assembly of the fertilization membrane of the sea urchin: Isolation of a divalent cation-dependent intermediate and its crosslinking in vitro

Cited by 46 publications

References 30 publications

Dtr1p, a Multidrug Resistance Transporter of the Major Facilitator Superfamily, Plays an Essential Role in Spore Wall Maturation in Saccharomyces cerevisiae

Dtr1p, a Multidrug Resistance Transporter of the Major Facilitator Superfamily, Plays an Essential Role in Spore Wall Maturation in Saccharomyces cerevisiae

Insights into the Molecular Mechanisms Involved in Sea Urchin Fertilization Envelope Assembly

Presence of a proteinase inhibitor in the vitelline envelope and its role in eggs of the fishTribolodon hakonensis

Contact Info

Product

Resources

About