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Disruption of blood-testis barrier dynamics in ether-lipid-deficient mice

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Abstract

One of the major roles of Sertoli cells is to establish the blood-testis (Sertoli cell) barrier (BTB), which is permanently assembled and disassembled to accommodate the translocation of leptotene spermatocytes from the basal into the adluminal compartment of the seminiferous epithelium and to guarantee completion of meiosis and spermiogenesis. Recently, we have demonstrated spermatogenesis to be arrested before spermatid elongation in Gnpat-null mice with selective deficiency of ether lipids (ELs) whose functions are poorly understood. In this study, we have focused on the spatio-temporal expression of several BTB tight-junctional proteins in the first wave of spermatogenesis to obtain insights into the physiological role of ELs during BTB establishment and dynamics. Our data confirm the transient existence of Russell’s intermediate or translocation compartment delineated by two separate claudin-3-positive luminal and basal tight junctions and reveal that EL deficiency blocks BTB remodeling. This block is associated with (1) downregulation and mistargeting of claudin-3 and (2) impaired BTB disassembly resulting in deficient sealing of the intermediate compartment as shown by increased BTB permeability to biotin. These results suggest that ELs are essential for cyclic BTB dynamics ensuring the sluice mechanism for leptotene translocation into the adluminal compartment.

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Abbreviations

AR:

androgen receptor

BTB:

blood-testis barrier

CAR:

coxsackie virus/adenovirus receptor

CK18:

cytokeratin 18

Cldn3:

claudin-3

Cldn11:

oligodendrocyte-specific protein/claudin-11

DA-GPE:

diacyl-glycerophosphorylethanolamine

ELs:

ether lipids

GalEAG:

precursor/degradative product of seminolipid

Gnpat (DAPAT):

dihydroxyacetonephosphate acyltransferase

PEs:

phosphatidylethanolamines

PlmGPEs:

plasmenyl-glycerophosphorylethanolamines, plasmenylethanolamines

PLs:

plasmalogens

SCARCO:

Sertoli-cell-selective androgen receptor knockout

SGalAAG:

seminolipid (3-sulfogalactosyl-1-alkyl-2-acyl-sn-glycerol, galactosylalkylacylglycerol (GalEAG) I3-sulfate)

TJs:

tight junctions

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Acknowledgments

The excellent technical assistance of Ingrid Kuhn-Krause is gratefully acknowledged. We thank Sven Weimann, Rolf Nonnenmacher, and Dr. Andreas Schober for help with the preparation of the figures, and Dr. Manuela Simoni, Centre of Reproductive Medicine and Andrology, University of Münster, 48149 Münster, Germany (present address: University of Modena and Reggio Emilia, Department of Medicine,Endocrinology, and Metabolism, 41100 Modena, Italy) for the determination of intratesticular testosterone and follicle-stimulating hormone levels. We are also grateful to Dr. Britta Brügger for making the triple Quadrupole nano-electrospray-ionization tandem mass spectrometry available to us.

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Authors and Affiliations

  1. Department of Anatomy and Medical Cell Biology, University of Heidelberg, Heidelberg, Germany

    Dorde Komljenovic & Karin Gorgas

  2. Department of Cellular and Molecular Pathology, German Cancer Research Center, Heidelberg, Germany

    Roger Sandhoff

  3. Heidelberg Center of Biochemistry (BZH), University of Heidelberg, Heidelberg, Germany

    Andre Teigler & Wilhelm W. Just

  4. Department of Cell Biology, German Cancer Research Center, Heidelberg, Germany

    Hans Heid

  5. Division of Medical Physics in Radiology, German Cancer Research Center, Heidelberg, Germany

    Dorde Komljenovic

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  1. Dorde Komljenovic
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  2. Roger Sandhoff
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  3. Andre Teigler
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  4. Hans Heid
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  5. Wilhelm W. Just
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  6. Karin Gorgas
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Corresponding authors

Correspondence to Roger Sandhoff, Wilhelm W. Just or Karin Gorgas.

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This work was supported by the German Research Foundation (grants Go 432/2-1, Ju 166/3-1, and Sa 172/1-1).

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Table S1

Mass spectrometric signal intensities of PlmGPEs (red) and DA-GPEs (green) in percent of total DA-GPE signal intensities in wild-type (WT) and mutant (KO) testis. A roughly seven-fold relative increase of the major testicular plasmenylethanolamines (PlmGPEs) as compared with diacyl-glycerophosphorylethanolamines (DA-GPEs) from postnatal day 6 (P6) to P30 could be detected, as could the complete loss of PlmGPEs in Gnpat-/- testis, taking the most abundant PlmGPEs (38:5 and 38:4; m/z 750 and 752) into more detailed consideration. The faint signals of PlmGPE species were within or slightly above background noise. T-test (two-tailed type 3 t-test); n.s not significant, *P<0.05, **P<0.01, ***P<0.001 (DOC 141 kb)

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Komljenovic, D., Sandhoff, R., Teigler, A. et al. Disruption of blood-testis barrier dynamics in ether-lipid-deficient mice. Cell Tissue Res 337, 281–299 (2009). https://doi.org/10.1007/s00441-009-0809-7

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