Cargando…

Yolk protein is expressed in the insect testis and interacts with sperm

BACKGROUND: Male and female gametes follow diverse developmental pathways dictated by their distinct roles in fertilization. While oocytes of oviparous animals accumulate yolk in the cytoplasm, spermatozoa slough off most of their cytoplasm in the process of individualization. Mammalian spermatozoa...

Descripción completa

Detalles Bibliográficos
Autores principales: Bebas, Piotr, Kotwica, Joanna, Joachimiak, Ewa, Giebultowicz, Jadwiga M
Formato: Texto
Lenguaje:English
Publicado: BioMed Central 2008
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2440742/
https://www.ncbi.nlm.nih.gov/pubmed/18549506
http://dx.doi.org/10.1186/1471-213X-8-64
_version_ 1782156569190858752
author Bebas, Piotr
Kotwica, Joanna
Joachimiak, Ewa
Giebultowicz, Jadwiga M
author_facet Bebas, Piotr
Kotwica, Joanna
Joachimiak, Ewa
Giebultowicz, Jadwiga M
author_sort Bebas, Piotr
collection PubMed
description BACKGROUND: Male and female gametes follow diverse developmental pathways dictated by their distinct roles in fertilization. While oocytes of oviparous animals accumulate yolk in the cytoplasm, spermatozoa slough off most of their cytoplasm in the process of individualization. Mammalian spermatozoa released from the testis undergo extensive modifications in the seminal ducts involving a variety of glycoproteins. Ultrastructural studies suggest that glycoproteins are involved in sperm maturation in insects; however, their characterization at the molecular level is lacking. We reported previously that the circadian clock controls sperm release and maturation in several insect species. In the moth, Spodoptera littoralis, the secretion of glycoproteins into the seminal fluid occurs in a daily rhythmic pattern. The purpose of this study was to characterize seminal fluid glycoproteins in this species and elucidate their role in the process of sperm maturation. RESULTS: We collected seminal fluid proteins from males before and after daily sperm release. These samples were separated by 2-D gel electrophoresis, and gels were treated with a glycoprotein-detecting probe. We observed a group of abundant glycoproteins in the sample collected after sperm release, which was absent in the sample collected before sperm release. Sequencing of these glycoproteins by mass spectroscopy revealed peptides bearing homology with components of yolk, which is known to accumulate in developing oocytes. This unexpected result was confirmed by Western blotting demonstrating that seminal fluid contains protein immunoreactive to antibody against yolk protein YP2 produced in the follicle cells surrounding developing oocytes. We cloned the fragment of yp2 cDNA from S. littoralis and determined that it is expressed in both ovaries and testes. yp2 mRNA and YP2 protein were detected in the somatic cyst cells enveloping sperm inside the testis. During the period of sperm release, YP2 protein appears in the seminal fluid and forms an external coat on spermatozoa. CONCLUSION: One of the yolk protein precursors YP2, which in females accumulate in the oocytes to provision developing embryos, appears to have a second male-specific role. It is produced in the testes and released into the seminal fluid where it interacts with sperm. These data reveal unexpected common factor in the maturation of insect eggs and sperm.
format Text
id pubmed-2440742
institution National Center for Biotechnology Information
language English
publishDate 2008
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-24407422008-06-27 Yolk protein is expressed in the insect testis and interacts with sperm Bebas, Piotr Kotwica, Joanna Joachimiak, Ewa Giebultowicz, Jadwiga M BMC Dev Biol Research Article BACKGROUND: Male and female gametes follow diverse developmental pathways dictated by their distinct roles in fertilization. While oocytes of oviparous animals accumulate yolk in the cytoplasm, spermatozoa slough off most of their cytoplasm in the process of individualization. Mammalian spermatozoa released from the testis undergo extensive modifications in the seminal ducts involving a variety of glycoproteins. Ultrastructural studies suggest that glycoproteins are involved in sperm maturation in insects; however, their characterization at the molecular level is lacking. We reported previously that the circadian clock controls sperm release and maturation in several insect species. In the moth, Spodoptera littoralis, the secretion of glycoproteins into the seminal fluid occurs in a daily rhythmic pattern. The purpose of this study was to characterize seminal fluid glycoproteins in this species and elucidate their role in the process of sperm maturation. RESULTS: We collected seminal fluid proteins from males before and after daily sperm release. These samples were separated by 2-D gel electrophoresis, and gels were treated with a glycoprotein-detecting probe. We observed a group of abundant glycoproteins in the sample collected after sperm release, which was absent in the sample collected before sperm release. Sequencing of these glycoproteins by mass spectroscopy revealed peptides bearing homology with components of yolk, which is known to accumulate in developing oocytes. This unexpected result was confirmed by Western blotting demonstrating that seminal fluid contains protein immunoreactive to antibody against yolk protein YP2 produced in the follicle cells surrounding developing oocytes. We cloned the fragment of yp2 cDNA from S. littoralis and determined that it is expressed in both ovaries and testes. yp2 mRNA and YP2 protein were detected in the somatic cyst cells enveloping sperm inside the testis. During the period of sperm release, YP2 protein appears in the seminal fluid and forms an external coat on spermatozoa. CONCLUSION: One of the yolk protein precursors YP2, which in females accumulate in the oocytes to provision developing embryos, appears to have a second male-specific role. It is produced in the testes and released into the seminal fluid where it interacts with sperm. These data reveal unexpected common factor in the maturation of insect eggs and sperm. BioMed Central 2008-06-13 /pmc/articles/PMC2440742/ /pubmed/18549506 http://dx.doi.org/10.1186/1471-213X-8-64 Text en Copyright © 2008 Bebas et al; licensee BioMed Central Ltd. http://creativecommons.org/licenses/by/2.0 This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( (http://creativecommons.org/licenses/by/2.0) ), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Article
Bebas, Piotr
Kotwica, Joanna
Joachimiak, Ewa
Giebultowicz, Jadwiga M
Yolk protein is expressed in the insect testis and interacts with sperm
title Yolk protein is expressed in the insect testis and interacts with sperm
title_full Yolk protein is expressed in the insect testis and interacts with sperm
title_fullStr Yolk protein is expressed in the insect testis and interacts with sperm
title_full_unstemmed Yolk protein is expressed in the insect testis and interacts with sperm
title_short Yolk protein is expressed in the insect testis and interacts with sperm
title_sort yolk protein is expressed in the insect testis and interacts with sperm
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2440742/
https://www.ncbi.nlm.nih.gov/pubmed/18549506
http://dx.doi.org/10.1186/1471-213X-8-64
work_keys_str_mv AT bebaspiotr yolkproteinisexpressedintheinsecttestisandinteractswithsperm
AT kotwicajoanna yolkproteinisexpressedintheinsecttestisandinteractswithsperm
AT joachimiakewa yolkproteinisexpressedintheinsecttestisandinteractswithsperm
AT giebultowiczjadwigam yolkproteinisexpressedintheinsecttestisandinteractswithsperm