Characteristics of the Epididymal Luminal Environment Responsible for Sperm Maturation and Storage

The testicular spermatozoa of all mammalian species are considered functionally immature owing to their inability to swim in a progressive manner and engage in productive interactions with the cumulus-oocyte complex. The ability to express these key functional attributes develops progressively durin...

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Published inFrontiers in endocrinology (Lausanne) Vol. 9; p. 59
Main Authors Zhou, Wei, De Iuliis, Geoffry N., Dun, Matthew D., Nixon, Brett
Format Journal Article
LanguageEnglish
Published Switzerland Frontiers Media S.A 28.02.2018
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Online AccessGet full text
ISSN1664-2392
1664-2392
DOI10.3389/fendo.2018.00059

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Abstract The testicular spermatozoa of all mammalian species are considered functionally immature owing to their inability to swim in a progressive manner and engage in productive interactions with the cumulus-oocyte complex. The ability to express these key functional attributes develops progressively during the cells' descent through the epididymis, a highly specialized ductal system that forms an integral part of the male reproductive tract. The functional maturation of the spermatozoon is achieved continuous interactions with the epididymal luminal microenvironment and remarkably, occurs in the complete absence of gene transcription or protein translation. Compositional analysis of the luminal fluids collected from the epididymis of a variety of species has revealed the complexity of this milieu, with a diversity of inorganic ions, proteins, and small non-coding RNA transcripts having been identified to date. Notably, both the quantitative and qualitative profile of each of these different luminal elements display substantial segment-to-segment variation, which in turn contribute to the regionalized functionality of this long tubule. Thus, spermatozoa acquire functional maturity in the proximal segments before being stored in a quiescent state in the distal segment in preparation for ejaculation. Such marked division of labor is achieved the combined secretory and absorptive activity of the epithelial cells lining each segment. Here, we review our current understanding of the molecular mechanisms that exert influence over the unique intraluminal environment of the epididymis, with a particular focus on vesicle-dependent mechanisms that facilitate intercellular communication between the epididymal soma and maturing sperm cell population.
AbstractList The testicular spermatozoa of all mammalian species are considered functionally immature owing to their inability to swim in a progressive manner and engage in productive interactions with the cumulus–oocyte complex. The ability to express these key functional attributes develops progressively during the cells’ descent through the epididymis, a highly specialized ductal system that forms an integral part of the male reproductive tract. The functional maturation of the spermatozoon is achieved via continuous interactions with the epididymal luminal microenvironment and remarkably, occurs in the complete absence of de novo gene transcription or protein translation. Compositional analysis of the luminal fluids collected from the epididymis of a variety of species has revealed the complexity of this milieu, with a diversity of inorganic ions, proteins, and small non-coding RNA transcripts having been identified to date. Notably, both the quantitative and qualitative profile of each of these different luminal elements display substantial segment-to-segment variation, which in turn contribute to the regionalized functionality of this long tubule. Thus, spermatozoa acquire functional maturity in the proximal segments before being stored in a quiescent state in the distal segment in preparation for ejaculation. Such marked division of labor is achieved via the combined secretory and absorptive activity of the epithelial cells lining each segment. Here, we review our current understanding of the molecular mechanisms that exert influence over the unique intraluminal environment of the epididymis, with a particular focus on vesicle-dependent mechanisms that facilitate intercellular communication between the epididymal soma and maturing sperm cell population.
The testicular spermatozoa of all mammalian species are considered functionally immature owing to their inability to swim in a progressive manner and engage in productive interactions with the cumulus-oocyte complex. The ability to express these key functional attributes develops progressively during the cells' descent through the epididymis, a highly specialized ductal system that forms an integral part of the male reproductive tract. The functional maturation of the spermatozoon is achieved continuous interactions with the epididymal luminal microenvironment and remarkably, occurs in the complete absence of gene transcription or protein translation. Compositional analysis of the luminal fluids collected from the epididymis of a variety of species has revealed the complexity of this milieu, with a diversity of inorganic ions, proteins, and small non-coding RNA transcripts having been identified to date. Notably, both the quantitative and qualitative profile of each of these different luminal elements display substantial segment-to-segment variation, which in turn contribute to the regionalized functionality of this long tubule. Thus, spermatozoa acquire functional maturity in the proximal segments before being stored in a quiescent state in the distal segment in preparation for ejaculation. Such marked division of labor is achieved the combined secretory and absorptive activity of the epithelial cells lining each segment. Here, we review our current understanding of the molecular mechanisms that exert influence over the unique intraluminal environment of the epididymis, with a particular focus on vesicle-dependent mechanisms that facilitate intercellular communication between the epididymal soma and maturing sperm cell population.
The testicular spermatozoa of all mammalian species are considered functionally immature owing to their inability to swim in a progressive manner and engage in productive interactions with the cumulus–oocyte complex. The ability to express these key functional attributes develops progressively during the cells’ descent through the epididymis, a highly specialized ductal system that forms an integral part of the male reproductive tract. The functional maturation of the spermatozoon is achieved via continuous interactions with the epididymal luminal microenvironment and remarkably, occurs in the complete absence of de novo gene transcription or protein translation. Compositional analysis of the luminal fluids collected from the epididymis of a variety of species has revealed the complexity of this milieu, with a diversity of inorganic ions, proteins, and small non-coding RNA transcripts having been identified to date. Notably, both the quantitative and qualitative profile of each of these different luminal elements display substantial segment-to-segment variation, which in turn contribute to the regionalized functionality of this long tubule. Thus, spermatozoa acquire functional maturity in the proximal segments before being stored in a quiescent state in the distal segment in preparation for ejaculation. Such marked division of labor is achieved via the combined secretory and absorptive activity of the epithelial cells lining each segment. Here, we review our current understanding of the molecular mechanisms that exert influence over the unique intraluminal environment of the epididymis, with a particular focus on vesicle-dependent mechanisms that facilitate intercellular communication between the epididymal soma and maturing sperm cell population.
The testicular spermatozoa of all mammalian species are considered functionally immature owing to their inability to swim in a progressive manner and engage in productive interactions with the cumulus-oocyte complex. The ability to express these key functional attributes develops progressively during the cells' descent through the epididymis, a highly specialized ductal system that forms an integral part of the male reproductive tract. The functional maturation of the spermatozoon is achieved via continuous interactions with the epididymal luminal microenvironment and remarkably, occurs in the complete absence of de novo gene transcription or protein translation. Compositional analysis of the luminal fluids collected from the epididymis of a variety of species has revealed the complexity of this milieu, with a diversity of inorganic ions, proteins, and small non-coding RNA transcripts having been identified to date. Notably, both the quantitative and qualitative profile of each of these different luminal elements display substantial segment-to-segment variation, which in turn contribute to the regionalized functionality of this long tubule. Thus, spermatozoa acquire functional maturity in the proximal segments before being stored in a quiescent state in the distal segment in preparation for ejaculation. Such marked division of labor is achieved via the combined secretory and absorptive activity of the epithelial cells lining each segment. Here, we review our current understanding of the molecular mechanisms that exert influence over the unique intraluminal environment of the epididymis, with a particular focus on vesicle-dependent mechanisms that facilitate intercellular communication between the epididymal soma and maturing sperm cell population.The testicular spermatozoa of all mammalian species are considered functionally immature owing to their inability to swim in a progressive manner and engage in productive interactions with the cumulus-oocyte complex. The ability to express these key functional attributes develops progressively during the cells' descent through the epididymis, a highly specialized ductal system that forms an integral part of the male reproductive tract. The functional maturation of the spermatozoon is achieved via continuous interactions with the epididymal luminal microenvironment and remarkably, occurs in the complete absence of de novo gene transcription or protein translation. Compositional analysis of the luminal fluids collected from the epididymis of a variety of species has revealed the complexity of this milieu, with a diversity of inorganic ions, proteins, and small non-coding RNA transcripts having been identified to date. Notably, both the quantitative and qualitative profile of each of these different luminal elements display substantial segment-to-segment variation, which in turn contribute to the regionalized functionality of this long tubule. Thus, spermatozoa acquire functional maturity in the proximal segments before being stored in a quiescent state in the distal segment in preparation for ejaculation. Such marked division of labor is achieved via the combined secretory and absorptive activity of the epithelial cells lining each segment. Here, we review our current understanding of the molecular mechanisms that exert influence over the unique intraluminal environment of the epididymis, with a particular focus on vesicle-dependent mechanisms that facilitate intercellular communication between the epididymal soma and maturing sperm cell population.
Author De Iuliis, Geoffry N.
Nixon, Brett
Dun, Matthew D.
Zhou, Wei
AuthorAffiliation 3 Cancer Research Program, School of Biomedical Sciences and Pharmacy, Hunter Medical Research Institute, University of Newcastle , New Lambton Heights, NSW , Australia
1 Priority Research Centre for Reproductive Science, School of Environmental and Life Sciences, University of Newcastle , Callaghan, NSW , Australia
2 Faculty of Health and Medicine, University of Newcastle , Callaghan, NSW , Australia
AuthorAffiliation_xml – name: 3 Cancer Research Program, School of Biomedical Sciences and Pharmacy, Hunter Medical Research Institute, University of Newcastle , New Lambton Heights, NSW , Australia
– name: 1 Priority Research Centre for Reproductive Science, School of Environmental and Life Sciences, University of Newcastle , Callaghan, NSW , Australia
– name: 2 Faculty of Health and Medicine, University of Newcastle , Callaghan, NSW , Australia
Author_xml – sequence: 1
  givenname: Wei
  surname: Zhou
  fullname: Zhou, Wei
– sequence: 2
  givenname: Geoffry N.
  surname: De Iuliis
  fullname: De Iuliis, Geoffry N.
– sequence: 3
  givenname: Matthew D.
  surname: Dun
  fullname: Dun, Matthew D.
– sequence: 4
  givenname: Brett
  surname: Nixon
  fullname: Nixon, Brett
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Copyright Copyright © 2018 Zhou, De Iuliis, Dun and Nixon. 2018 Zhou, De Iuliis, Dun and Nixon
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Keywords apocrine secretion
intracellular communication
protein trafficking
epididymis
merocrine secretion
sperm maturation
epididymosome
dynamin
Language English
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Specialty section: This article was submitted to Reproduction, a section of the journal Frontiers in Endocrinology
Edited by: Marc Yeste, University of Girona, Spain
Reviewed by: Robert Sullivan, Laval University, Canada; Jean-Louis Dacheux, UMR7247 Physiologie de la reproduction et des comportements (PRC), France
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PublicationTitle Frontiers in endocrinology (Lausanne)
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Snippet The testicular spermatozoa of all mammalian species are considered functionally immature owing to their inability to swim in a progressive manner and engage in...
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StartPage 59
SubjectTerms apocrine secretion
Endocrinology
epididymis
intracellular communication
merocrine secretion
protein trafficking
sperm maturation
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Title Characteristics of the Epididymal Luminal Environment Responsible for Sperm Maturation and Storage
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