Register      Login
Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Lonidamine-ethyl ester-mediated remodelling of the Sertoli cell cytoskeleton induces phosphorylation of plakoglobin and promotes its interaction with α-catenin at the blood–testis barrier

Dolores D. Mruk A D , Michele Bonanomi B C and Bruno Silvestrini B C
+ Author Affiliations
- Author Affiliations

A Center for Biomedical Research, Population Council, 1230 York Avenue, New York, NY 10065, USA.

B S.B.M. Srl–Science of Biology in Medicine, Via Domenico Tardini 35-00167 Rome, Italy.

C Noopolis Foundation, Via Domenico Tardini 35-00167, Rome, Italy.

D Corresponding author. Email: mruk@popcbr.rockefeller.edu

Reproduction, Fertility and Development 29(5) 998-1011 https://doi.org/10.1071/RD15378
Submitted: 20 September 2015  Accepted: 27 January 2016   Published: 7 March 2016

Abstract

Several compounds affect male fertility by disrupting the adhesion of germ cells to Sertoli cells, which results in the release of undeveloped germ cells into the seminiferous tubule lumen that are incapable of fertilising the ovum. Indazole carboxylic acids are one class of compounds exhibiting such effects and they have been investigated as non-hormonal contraceptives for potential human use. The aims of this study were to investigate the effects of lonidamine-ethyl ester, an indazole carboxylic acid, on spermatogenesis and cell junctions, in particular, desmosomes. We found two doses of lonidamine-ethyl ester at 50 mg kg–1 to disrupt Sertoli–germ cell adhesion. By light and fluorescent microscopy, pronounced changes were observed in the distribution of actin microfilaments and intermediate filaments, as well as in the localisation of plakoglobin, a protein with structural and signalling roles at the desmosome and adherens junction at the blood–testis barrier. Furthermore, immunoblotting and immunoprecipitation experiments using testis lysates revealed a significant upregulation (P < 0.01) of plakoglobin and Tyr-phosphorylated plakoglobin. Co-immunoprecipitation experiments showed an increase in the interaction between plakoglobin and fyn proto-oncogene, an Src family non-receptor tyrosine kinase, after treatment, as well as an increase in the interaction between plakoglobin and α-catenin. Taken collectively, these data indicate that a disruption of Sertoli cell and spermatocyte–spermatid adhesion in the seminiferous epithelium by lonidamine-ethyl ester results in the phosphorylation of plakoglobin, thereby promoting its interaction with α-catenin at the blood–testis barrier.

Additional keywords: adjudin, male contraception, spermatogenesis.


References

Bignold, L. P. (2006). Alkylating agents and DNA polymerases. Anticancer Res. 26, 1327–1336.
| 1:CAS:528:DC%2BD28XktVGrur0%3D&md5=96fc5ec0d47c5da63f7e2d338044588fCAS | 16619541PubMed |

Borradori, L., and Sonnenberg, A. (1999). Structure and function of hemidesmosomes: more than simple adhesion complexes. J. Invest. Dermatol. 112, 411–418.
Structure and function of hemidesmosomes: more than simple adhesion complexes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXit1Ojtro%3D&md5=4a60a143241bda1ff3a61c53777dbebbCAS | 10201522PubMed |

Brawer, M. K. (2005). Lonidamine: basic science and rationale for treatment of prostatic proliferative disorders. Rev. Urol. 7, S21–S26.
| 16986057PubMed |

Byers, S. W., Sujarit, S., Jegou, B., Butz, S., Hoschutzky, H., Herrenknecht, K., MacCalman, C., and Blaschuk, O. W. (1994). Cadherins and cadherin-associated molecules in the developing and maturing rat testis. Endocrinology 134, 630–639.
| 1:CAS:528:DyaK2cXhvVOqur8%3D&md5=2c2e561a1a19d4fb58246c155218de3fCAS | 7507830PubMed |

Cadigan, K. M., and Peifer, M. (2009). Wnt signalling from development to disease: insights from model systems. Cold Spring Harb. Perspect. Biol. 1, a002881.
Wnt signalling from development to disease: insights from model systems.Crossref | GoogleScholarGoogle Scholar | 20066091PubMed |

Caputo, A., and Silvestrini, B. (1984). Lonidamine, a new approach to cancer therapy. Oncology 41, 2–6.
Lonidamine, a new approach to cancer therapy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXktFKmtb8%3D&md5=4ca9f3b283dcfbb04f55a93716e896feCAS | 6371644PubMed |

Chen, Y. M., Lee, N. P. Y., Mruk, D. D., Lee, W. M., and Cheng, C. Y. (2003). Fer kinase/Fer T and adherens junction dynamics in the testis: an in vitro and in vivo study. Biol. Reprod. 69, 656–672.
Fer kinase/Fer T and adherens junction dynamics in the testis: an in vitro and in vivo study.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXlvVeru7s%3D&md5=70a117f1563a12274db0692ba60b290aCAS | 12700184PubMed |

Cheng, C. Y., Silvestrini, B., Grima, J., Mo, M. Y., Zhu, L. J., Johansson, E., Saso, L., Leone, M. G., Palmery, M., and Mruk, D. (2001). Two new male contraceptives exert their effects by depleting germ cells prematurely from the testis. Biol. Reprod. 65, 449–461.
Two new male contraceptives exert their effects by depleting germ cells prematurely from the testis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXls1Wgu7c%3D&md5=aad329426e75642ae61a71a07ffe5f2fCAS | 11466213PubMed |

Cheng, C. Y., Mo, M. Y., Grima, J., Saso, L., Tita, B., Mruk, D., and Silvestrini, B. (2002). Indazole carboxylic acids in male contraception. Contraception 65, 265–268.
Indazole carboxylic acids in male contraception.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XjvVSnsbw%3D&md5=403806237567ad43a30f8ecbb8481e6fCAS | 12020774PubMed |

De Martino, C., Malcorni, W., Bellocci, M., Floridi, A., and Marcante, M. L. (1981). Effects of AF1312 TS and lonidamine on mammalian testis. A morphological study. Chemotherapy 27, 27–42.
Effects of AF1312 TS and lonidamine on mammalian testis. A morphological study.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38XivVyhuw%3D%3D&md5=a481d587c6428f5027fea4a7ad91d94cCAS | 7285636PubMed |

Di Cosimo, S., Ferretti, G., Papaldo, P., Carlini, P., Fabi, A., and Cognetti, F. (2003). Lonidamine: efficacy and safety in clinical trials for the treatment of solid tumours. Drugs Today (Barc) 39, 157–174.
Lonidamine: efficacy and safety in clinical trials for the treatment of solid tumours.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXktF2gsLs%3D&md5=189ed20058a37b20734f1891a3f7063cCAS | 12730701PubMed |

Dupin, I., and Etienne-Manneville, S. (2011). Nuclear positioning: mechanisms and functions. Int. J. Biochem. Cell Biol. 43, 1698–1707.
Nuclear positioning: mechanisms and functions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtl2gsrjN&md5=25d728181363a61354cc45e2b2670c4bCAS | 21959251PubMed |

Ellenbroek, S. I., Iden, S., and Collard, J. G. (2012). Cell polarity proteins and cancer. Semin. Cancer Biol. 22, 208–215.
Cell polarity proteins and cancer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xnt12kur0%3D&md5=18fa8900beb38f4b4916bb68eb8a46e7CAS | 22465739PubMed |

Floridi, A., Paggi, M. G., D’Atri, S., DeMartino, C., Marcante, M. L., Silvestrini, B., and Caputo, A. (1981a). Effect of lonidamine on the energy metabolism of Ehrlich ascites tumour cells. Cancer Res. 41, 4661–4666.
| 1:CAS:528:DyaL38Xktl0%3D&md5=9226690adf3ece5009cc0e4276d9a2cfCAS | 7306982PubMed |

Floridi, A., Paggi, M. G., Marcante, M. L., Silvestrini, B., Caputo, A., and De Martino, C. (1981b). Lonidamine, a selective inhibitor of aerobic glycolysis of murine tumour cells. J. Natl. Cancer Inst. 66, 497–499.
| 1:CAS:528:DyaL3MXhsFSit70%3D&md5=16ccca66269543318e9dcb4cf645d8adCAS | 6937706PubMed |

Fu, D., Calvo, J. A., and Samson, L. D. (2012). Balancing repair and tolerance of DNA damage caused by alkylating agents. Nat. Rev. Cancer 12, 104–120.
| 1:CAS:528:DC%2BC38XlsFygtQ%3D%3D&md5=8a40bdf776469c154bfdd81a726321ddCAS | 22237395PubMed |

Gödde, N. J., Pearson, H. B., Smith, L. K., and Humbert, P. O. (2014). Dissecting the role of polarity regulators in cancer through the use of mouse models. Exp. Cell Res. 328, 249–257.
Dissecting the role of polarity regulators in cancer through the use of mouse models.Crossref | GoogleScholarGoogle Scholar | 25179759PubMed |

Green, K. J., Getsios, S., Troyanovsky, S., and Godsel, L. M. (2010). Intercellular junction assembly, dynamics and homeostasis. Cold Spring Harb. Perspect. Biol. 2, a000125.
Intercellular junction assembly, dynamics and homeostasis.Crossref | GoogleScholarGoogle Scholar | 20182611PubMed |

Grima, J., Silvestrini, B., and Cheng, C. Y. (2001). Reversible inhibition of spermatogenesis in rats using a new male contraceptive, 1-(2,4-dichlorobenzyl)-indazole-3-carbohydrazide. Biol. Reprod. 64, 1500–1508.
Reversible inhibition of spermatogenesis in rats using a new male contraceptive, 1-(2,4-dichlorobenzyl)-indazole-3-carbohydrazide.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjtFKqs7c%3D&md5=d450debbacd9393b3064c7511ac426acCAS | 11319158PubMed |

Hu, G. X., Hu, L. F., Yang, D. Z., Li, J. W., Chen, G. R., Chen, B. B., Mruk, D. D., Bonanomi, M., Silvestrini, B., Cheng, C. Y., and Ge, R. S. (2009). Adjudin targeting rabbit germ cell adhesion as a male contraceptive: a pharmacokinetic study. J. Androl. 30, 87–93.
Adjudin targeting rabbit germ cell adhesion as a male contraceptive: a pharmacokinetic study.Crossref | GoogleScholarGoogle Scholar | 18802200PubMed |

Kopera, I. A., Su, L., Bilinska, B., Cheng, C. Y., and Mruk, D. D. (2009). An in vivo study on adjudin and blood–testis barrier dynamics. Endocrinology 150, 4724–4733.
An in vivo study on adjudin and blood–testis barrier dynamics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXht1OktrvI&md5=de0735ec5bd291770add3d62e106f700CAS | 19574397PubMed |

Kowalczyk, A. P., and Green, K. J. (2013). Structure, function and regulation of desmosomes. Prog. Mol. Biol. Transl. Sci. 116, 95–118.
Structure, function and regulation of desmosomes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXpsVOru70%3D&md5=b40f2833f841f7006321ddc4e7b3b650CAS | 23481192PubMed |

Küppers, V., Vockel, M., Nottebaum, A. F., and Vestweber, D. (2014). Phosphatases and kinases as regulators of the endothelial barrier function. Cell Tissue Res. 355, 577–586.
Phosphatases and kinases as regulators of the endothelial barrier function.Crossref | GoogleScholarGoogle Scholar | 24566520PubMed |

Li, S., and Huang, L. (1997). In vivo gene transfer via intravenous administration of cationic lipid–protamine–DNA (LPD) complexes. Gene Ther. 4, 891–900.
In vivo gene transfer via intravenous administration of cationic lipid–protamine–DNA (LPD) complexes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXmtVSkurY%3D&md5=c88d71a11f1e159849fe1f618b4b00beCAS | 9349425PubMed |

Li, S., Rizzo, M. A., Bhattacharya, S., and Huang, L. (1998). Characterisation of cationic lipid–protamine–DNA (LPD) complexes for intravenous gene delivery. Gene Ther. 5, 930–937.
Characterisation of cationic lipid–protamine–DNA (LPD) complexes for intravenous gene delivery.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXksFWkurk%3D&md5=4380cd8d9a5d428932271517bfb795f9CAS | 9813664PubMed |

Lie, P. P. Y., Cheng, C. Y., and Mruk, D. D. (2010). The desmoglein-2/desmocollin-2/Src kinase protein complex regulates blood–testis barrier dynamics. Int. J. Biochem. Cell Biol. 42, 975–986.
The desmoglein-2/desmocollin-2/Src kinase protein complex regulates blood–testis barrier dynamics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXlsFKmsbo%3D&md5=9f27c82640f22b78d359c1f99e2346d1CAS |

Lie, P. P. Y., Cheng, C. Y., and Mruk, D. D. (2011). The biology of the desmosome-like junction: a versatile anchoring junction and signal transducer in the seminiferous epithelium. Int. Rev. Cell Mol. Biol. 286, 223–269.
The biology of the desmosome-like junction: a versatile anchoring junction and signal transducer in the seminiferous epithelium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXksFSks7k%3D&md5=2ddc4fc516a50f270d65d7bbb1b8500dCAS |

Malorni, W., Meschini, S., Matarrese, P., and Arancia, G. (1992). The cytoskeleton as a subcellular target of the antineoplastic drug lonidamine. Anticancer Res. 12, 2037–2045.
| 1:CAS:528:DyaK3sXitVCrsbg%3D&md5=ea1705ecf77d6cd9e4fee2be3c2809c7CAS | 1295447PubMed |

Maranghi, F., Mantovani, A., Macri, C., Romeo, A., Eleuteri, P., Leter, G., Rescis, M., Spano, M., and Saso, L. (2005). Long-term effects of lonidamine on mouse testes. Contraception 72, 268–272.
Long-term effects of lonidamine on mouse testes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVeiu7fK&md5=454f13a53f05dc69f91ae6fd21db2390CAS | 16181970PubMed |

Mathupala, S. P., Ko, Y. H., and Pedersen, P. L. (2010). The pivotal roles of mitochondria in cancer: Warburg and beyond and encouraging prospects for effective therapies. Biochim. Biophys. Acta 1797, 1225–1230.
The pivotal roles of mitochondria in cancer: Warburg and beyond and encouraging prospects for effective therapies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXnvV2ru7w%3D&md5=ffaa4d59b7c9ec2b9c249b49ffd97166CAS | 20381449PubMed |

McCole, D. F. (2013). Phosphatase regulation of intercellular junctions. Tissue Barriers 1, e26713.
Phosphatase regulation of intercellular junctions.Crossref | GoogleScholarGoogle Scholar | 24868494PubMed |

Miccoli, L., Poirson-Bichat, F., Sureau, F., Goncalves, R. B., Bourgeois, Y., Dutrillaux, B., Poupon, M. F., and Oudard, S. (1998). Potentiation of lonidamine and diazepam, two agents acting on mitochondria, in human glioblastoma treatment. J. Natl. Cancer Inst. 90, 1400–1406.
Potentiation of lonidamine and diazepam, two agents acting on mitochondria, in human glioblastoma treatment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXmtlelu74%3D&md5=b286ccb79fac05da8f8c7000eb740a4bCAS | 9747871PubMed |

Miravet, S., Piedra, J., Castano, J., Raurell, I., Franci, C., Dunach, M., and Garcia de Herreros, A. (2003). Tyrosine phosphorylation of plakoglobin causes contrary effects on its association with desmosomes and adherens junction components and modulates β-catenin-mediated transcription. Mol. Cell. Biol. 23, 7391–7402.
Tyrosine phosphorylation of plakoglobin causes contrary effects on its association with desmosomes and adherens junction components and modulates β-catenin-mediated transcription.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXotVSru7c%3D&md5=f50cafa9542bee0ad6af32d2d1025232CAS | 14517306PubMed |

Mruk, D. D., and Cheng, C. Y. (2004a). Cell–cell interactions at the ectoplasmic specialisation in the testis. Trends Endocrinol. Metab. 15, 439–447.
Cell–cell interactions at the ectoplasmic specialisation in the testis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXptFOmurs%3D&md5=e1e68d158091581f377e99eab60f808aCAS | 15519891PubMed |

Mruk, D. D., and Cheng, C. Y. (2004b). Sertoli–Sertoli and Sertoli–germ cell interactions and their significance in germ cell movement in the seminiferous epithelium during spermatogenesis. Endocr. Rev. 25, 747–806.
Sertoli–Sertoli and Sertoli–germ cell interactions and their significance in germ cell movement in the seminiferous epithelium during spermatogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVSjtrnP&md5=a5aebcec96bc23e27893b1c309b2a6baCAS | 15466940PubMed |

Mruk, D. D., and Cheng, C. Y. (2011). Enhanced chemiluminescence (ECL) for routine immunoblotting: an inexpensive alternative to commercially available kits. Spermatogenesis 1, 121–122.
Enhanced chemiluminescence (ECL) for routine immunoblotting: an inexpensive alternative to commercially available kits.Crossref | GoogleScholarGoogle Scholar | 22319660PubMed |

Mruk, D. D., Wong, C. H., Silvestrini, B., and Cheng, C. Y. (2006). A male contraceptive targeting germ cell adhesion. Nat. Med. 12, 1323–1328.
A male contraceptive targeting germ cell adhesion.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFKlsLbM&md5=e161c96edb2babb998e9e3b89c513f1aCAS | 17072312PubMed |

Mruk, D. D., Silvestrini, B., and Cheng, C. Y. (2008). Anchoring junctions as drug targets: role in contraceptive development. Pharmacol. Rev. 60, 146–180.
Anchoring junctions as drug targets: role in contraceptive development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXitlWlsr8%3D&md5=99aa029e43fc14eb6eb0833cdb0f7ec7CAS | 18483144PubMed |

Muñoz-Pinedo, C., Mjiyad, N. E., and Ricci, J.-E. (2012). Cancer metabolism: current perspectives and future directions. Cell Death Dis. 3, e248.
Cancer metabolism: current perspectives and future directions.Crossref | GoogleScholarGoogle Scholar | 22237205PubMed |

Ning, S. C., and Hahn, G. M. (1990). Cytotoxicity of lonidamine alone and in combination with other drugs against murine RIF-1 and human HT1080 cells in vitro. Cancer Res. 50, 7867–7870.
| 1:CAS:528:DyaK3MXjsFGksA%3D%3D&md5=7181413e89b5301531fe1aeb1836cc9cCAS | 2253227PubMed |

Paranko, J., Kallajoki, M., Pelliniemi, L. J., Lehto, V. P., and Virtanen, I. (1986). Transient coexpression of cytokeratin and vimentin in differentiating rat Sertoli cells. Dev. Biol. 117, 35–44.
Transient coexpression of cytokeratin and vimentin in differentiating rat Sertoli cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28Xls12ls7w%3D&md5=fc1293fd89367bb545d9e2279480409fCAS | 2427374PubMed |

Price, G. S., Page, R. L., Riviere, J. E., Cline, J. M., and Thrall, D. E. (1996). Pharmacokinetics and toxicity of oral and intravenous lonidamine in dogs. Cancer Chemother. Pharmacol. 38, 129–135.
Pharmacokinetics and toxicity of oral and intravenous lonidamine in dogs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XjslCls7c%3D&md5=143abe5168a99b0a8ecd972af1ba1c70CAS | 8616902PubMed |

Rosenbluh, J., Wang, X., and Hahn, W. C. (2014). Genomic insights into WNT/β-catenin signalling. Trends Pharmacol. Sci. 35, 103–109.
Genomic insights into WNT/β-catenin signalling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXitVSgs7fK&md5=bcb07a01be46d0d3137978d2395359faCAS | 24365576PubMed |

Russell, L. (1977a). Desmosome-like junctions between Sertoli and germ cells in the rat testis. Am. J. Anat. 148, 301–312.
Desmosome-like junctions between Sertoli and germ cells in the rat testis.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE2s7nvFSmsA%3D%3D&md5=a4732d89e5dfc6af1c9ac5f22d542768CAS | 857631PubMed |

Russell, L. (1977b). Movement of spermatocytes from the basal to the adluminal compartment of the rat testis. Am. J. Anat. 148, 313–328.
Movement of spermatocytes from the basal to the adluminal compartment of the rat testis.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE2s7nvFSmsQ%3D%3D&md5=8ea41fef9c2f767a69e84358403810eaCAS | 857632PubMed |

Russell, L. D. (1993). Morphological and functional evidence for Sertoli–germ cell relationships. In ‘The Sertoli Cell’. (Eds L. D. Russell, M. D. Griswold.) pp. 365–390. (Cache River Press: Clearwater, FL.)

Savini, S., Zoli, W., Nanni, O., Volpi, A., Frassineti, G. L., Magni, E., Flamigni, A., Amadori, A., and Amadori, D. (1992). In vitro potentiation by lonidamine of the cytotoxic effect of adriamycin on primary and established breast cancer cell lines. Breast Cancer Res. Treat. 24, 27–34.
In vitro potentiation by lonidamine of the cytotoxic effect of adriamycin on primary and established breast cancer cell lines.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXhtl2gtL4%3D&md5=2e114bd0b08905fb45698ec9df82e0f9CAS | 1463869PubMed |

Tojkander, S., Gateva, G., and Lappalainen, P. (2012). Actin stress fibres – assembly, dynamics and biological roles. J. Cell Sci. 125, 1855–1864.
Actin stress fibres – assembly, dynamics and biological roles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVGltrzF&md5=2a2dc891dd4402123acc5c8be92c28b5CAS | 22544950PubMed |

Toyama, Y. (1976). Actin-like filaments in the Sertoli cell junctional specialisations in the swine and mouse testis. Anat. Rec. 186, 477–491.
Actin-like filaments in the Sertoli cell junctional specialisations in the swine and mouse testis.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE2s%2FosFKgug%3D%3D&md5=f515251972d0ae3131f5100531deb8b3CAS | 795323PubMed |

Traina, M. E., Guarino, M., Urbani, E., Saso, L., Eleuteri, P., Cordelli, E., Rescia, M., Leter, G., and Spano, M. (2005). Lonidamine transiently affects spermatogenesis in pubertal CD1 mice. Contraception 72, 262–267.
Lonidamine transiently affects spermatogenesis in pubertal CD1 mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVeiu7fJ&md5=d4ca652f069ecf3ed3d3a62ccbc98478CAS | 16181969PubMed |

Traina, M. E., Guarino, M., Natoli, A., Romeo, A., and Urbani, E. (2007). Lonidamine affects testicular steroid hormones in immature mice. Toxicol. Appl. Pharmacol. 221, 95–101.
Lonidamine affects testicular steroid hormones in immature mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXltF2ksLs%3D&md5=0dcafdfaca9aae9312fb47f08da49823CAS | 17442358PubMed |

Vogl, A. W., and Soucy, L. J. (1985). Arrangement and possible function of actin filament bundles in ectoplasmic specialisations of ground squirrel Sertoli cells. J. Cell Biol. 100, 814–825.
Arrangement and possible function of actin filament bundles in ectoplasmic specialisations of ground squirrel Sertoli cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXht12gtr8%3D&md5=20769fe6d5144fb3e337549a508964a3CAS | 3882723PubMed |

Vogl, A. W., Vaid, K. S., and Guttman, J. A. (2008). The Sertoli cell cytoskeleton. In ‘Molecular Mechanisms in Spermatogenesis’. (Ed. C. Y. Cheng.) pp. 186–211. (Landes Bioscience and Springer Science+Business Media: Austin, TX, USA.)

Wolosewick, J. J., De Mey, J., and Meininger, V. (1984). Ultrastructural localisation of tubulin and actin in polyethylene glycol-embedded rat seminiferous epithelium by immunogold staining. Biol. Cell 49, 219–226.
Ultrastructural localisation of tubulin and actin in polyethylene glycol-embedded rat seminiferous epithelium by immunogold staining.Crossref | GoogleScholarGoogle Scholar |

Yan, H. H. N., and Cheng, C. Y. (2005). Blood–testis barrier dynamics are regulated by an engagement–disengagement mechanism between tight and adherens junctions via peripheral adaptors. Proc. Natl. Acad. Sci. USA 102, 11722–11727.
Blood–testis barrier dynamics are regulated by an engagement–disengagement mechanism between tight and adherens junctions via peripheral adaptors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXpsFGgt7g%3D&md5=709f6090f1998820ed7667c39935501dCAS |

You, H., Lei, P., and Andreadis, S. T. (2013). JNK is a novel regulator of intercellular adhesion. Tissue Barriers 1, e26845.
JNK is a novel regulator of intercellular adhesion.Crossref | GoogleScholarGoogle Scholar | 24868495PubMed |

Zhurinsky, J., Shtutman, M., and Ben-Ze’ev, A. (2000). Plakoglobin and β-catenin: protein interactions, regulation and biological roles. J. Cell Sci. 113, 3127–3139.
| 1:CAS:528:DC%2BD3cXnsVyltL4%3D&md5=39ed6d748fa59b558f20b226e9d8e626CAS | 10954412PubMed |