3,981
Views
88
CrossRef citations to date
0
Altmetric
Basic Research Paper

Autophagy is required for ectoplasmic specialization assembly in sertoli cells

, , , , , , , , , , , & show all
Pages 814-832 | Received 29 Jun 2015, Accepted 23 Feb 2016, Published online: 12 Apr 2016

References

  • Roosen-Runge EC. The process of spermatogenesis in mammals. Biol Rev Camb Philos Soc 1962; 37:343-77; PMID:14493721; http://dx.doi.org/10.1111/j.1469-185X.1962.tb01616.x
  • Hess RA, Renato de Franca L. Spermatogenesis and cycle of the seminiferous epithelium. Advan Exp Med Biol 2008; 636:1-15; PMID:19856159; http://dx.doi.org/10.1007/978-0-387-09597-4_1
  • Griswold MD. The central role of Sertoli cells in spermatogenesis. Semin Cell Dev Biol 1998; 9:411-6; PMID:9813187; http://dx.doi.org/10.1006/scdb.1998.0203
  • Hai Y, Hou J, Liu Y, Yang H, Li Z, He Z. The roles and regulation of Sertoli cells in fate determinations of spermatogonial stem cells and spermatogenesis. Semin Cell Dev Biol 2014; 29:66-75; PMID:24718316; http://dx.doi.org/10.1016/j.semcdb.2014.04.007
  • Jegou B. The Sertoli-germ cell communication network in mammals. Int Rev Cytol 1993; 147:25-96; PMID:8225836; http://dx.doi.org/10.1016/S0074-7696(08)60766-4
  • Berruti G, Paiardi C. The dynamic of the apical ectoplasmic specialization between spermatids and Sertoli cells: the case of the small GTPase Rap1. Bio Med Res Int 2014; 2014:635979; PMID:24719879; http://dx.doi.org/10.1155/2014/635979
  • Kopera IA, Bilinska B, Cheng CY, Mruk DD. Sertoli-germ cell junctions in the testis: a review of recent data. Philos Trans R Soc Lond B Biol Sci 2010; 365:1593-605; PMID:20403872; http://dx.doi.org/10.1098/rstb.2009.0251
  • Lie PP, Cheng CY, Mruk DD. The biology of the desmosome-like junction a versatile anchoring junction and signal transducer in the seminiferous epithelium. Int Rev Cell Mol Biol 2011; 286:223-69; PMID:21199783; http://dx.doi.org/10.1016/B978-0-12-385859-7.00005-7
  • Qian X, Mruk DD, Cheng YH, Tang EI, Han D, Lee WM, Wong EW, Cheng CY. Actin binding proteins, spermatid transport and spermiation. Semin Cell Dev Biol 2014; 30:75-85; PMID:24735648; http://dx.doi.org/10.1016/j.semcdb.2014.04.018
  • Toyama Y, Maekawa M, Yuasa S. Ectoplasmic specializations in the Sertoli cell: new vistas based on genetic defects and testicular toxicology. Anat Sci Int 2003; 78:1-16; PMID:12680465; http://dx.doi.org/10.1046/j.0022-7722.2003.00034.x
  • Wong EW, Mruk DD, Cheng CY. Biology and regulation of ectoplasmic specialization, an atypical adherens junction type, in the testis. Biochimica et biophysica acta 2008; 1778:692-708; PMID:18068662; http://dx.doi.org/10.1016/j.bbamem.2007.11.006
  • Cheng CY, Mruk DD. The blood-testis barrier and its implications for male contraception. Pharmacol Rev 2012; 64:16-64; PMID:22039149; http://dx.doi.org/10.1124/pr.110.002790
  • Mruk DD, Cheng CY. Cell-cell interactions at the ectoplasmic specialization in the testis. Trends in endocrinology and metabolism: TEM 2004; 15:439-47; PMID:15519891; http://dx.doi.org/10.1016/S1043-2760(04)00219-X
  • Lee NP, Cheng CY. Ectoplasmic specialization, a testis-specific cell-cell actin-based adherens junction type: is this a potential target for male contraceptive development? Human reproduction update 2004; 10:349-69; PMID:15192055; http://dx.doi.org/10.1093/humupd/dmh026
  • Cheng CY, Mruk DD. Cell junction dynamics in the testis: Sertoli-germ cell interactions and male contraceptive development. Physiological reviews 2002; 82:825-74; PMID:12270945; http://dx.doi.org/10.1152/physrev.00009.2002
  • Li SY, Mruk DD, Cheng CY. Focal adhesion kinase is a regulator of F-actin dynamics: New insights from studies in the testis. Spermatogenesis 2013; 3:e25385; PMID:24381802; http://dx.doi.org/10.4161/spmg.25385
  • Mruk DD, Silvestrini B, Cheng CY. Anchoring junctions as drug targets: role in contraceptive development. Pharmacological reviews 2008; 60:146-80; PMID:18483144; http://dx.doi.org/10.1124/pr.107.07105
  • O'Donnell L, Nicholls PK, O'Bryan MK, McLachlan RI, Stanton PG. Spermiation: The process of sperm release. Spermatogenesis 2011; 1:14-35; PMID:21866274; http://dx.doi.org/10.4161/spmg.1.1.14525
  • Sperry AO. The dynamic cytoskeleton of the developing male germ cell. Biol Cell 2012; 104:297-305; PMID:22276751; http://dx.doi.org/10.1111/boc.201100102
  • Mizushima N, Yoshimori T, Ohsumi Y. The role of Atg proteins in autophagosome formation. Ann Rev Cell Dev Biol 2011; 27:107-32; PMID:21801009; http://dx.doi.org/10.1146/annurev-cellbio-092910-154005
  • Mizushima N, Levine B. Autophagy in mammalian development and differentiation. Nat Cell Biol 2010; 12:823-30; PMID:20811354; http://dx.doi.org/10.1038/ncb0910-823
  • Yang Z, Klionsky DJ. An overview of the molecular mechanism of autophagy. Curr Top Microbiol Immunol 2009; 335:1-32; PMID:19802558
  • Wang H, Wan H, Li X, Liu W, Chen Q, Wang Y, Yang L, Tang H, Zhang X, Duan E, et al. Atg7 is required for acrosome biogenesis during spermatogenesis in mice. Cell Res 2014; 24:852-69; PMID:24853953; http://dx.doi.org/10.1038/cr.2014.70
  • Tang Z, Lin MG, Stowe TR, Chen S, Zhu M, Stearns T, Franco B, Zhong Q. Autophagy promotes primary ciliogenesis by removing OFD1 from centriolar satellites. Nature 2013; 502:254-7; PMID:24089205; http://dx.doi.org/10.1038/nature12606
  • Mizushima N, Komatsu M. Autophagy: renovation of cells and tissues. Cell 2011; 147:728-41; PMID:22078875; http://dx.doi.org/10.1016/j.cell.2011.10.026
  • Ma Y, Yang HZ, Xu LM, Huang YR, Dai HL, Kang XN. Testosterone regulates the autophagic clearance of androgen binding protein in rat Sertoli cells. Scientific Reports 2015; 5:8894; PMID:25745956; http://dx.doi.org/10.1038/srep08894
  • Yefimova MG, Messaddeq N, Harnois T, Meunier AC, Clarhaut J, Noblanc A, Weickert JL, Cantereau A, Philippe M, Bourmeyster N, et al. A chimerical phagocytosis model reveals the recruitment by Sertoli cells of autophagy for the degradation of ingested illegitimate substrates. Autophagy 2013; 9:653-66; PMID:23439251; http://dx.doi.org/10.4161/auto.23839
  • Chen Y, Zhou Y, Wang X, Qian W, Han X. Microcystin-LR induces autophagy and apoptosis in rat Sertoli cells in vitro. Toxicon 2013; 76:84-93; PMID:24047964; http://dx.doi.org/10.1016/j.toxicon.2013.09.005
  • Eid N, Ito Y, Otsuki Y. Enhanced mitophagy in Sertoli cells of ethanol-treated rats: morphological evidence and clinical relevance. J Mol Histol 2012; 43:71-80; PMID:22076330; http://dx.doi.org/10.1007/s10735-011-9372-0
  • Hara T, Nakamura K, Matsui M, Yamamoto A, Nakahara Y, Suzuki-Migishima R, Yokoyama M, Mishima K, Saito I, Okano H, et al. Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice. Nature 2006; 441:885-9; PMID:16625204; http://dx.doi.org/10.1038/nature04724
  • Komatsu M, Waguri S, Ueno T, Iwata J, Murata S, Tanida I, Ezaki J, Mizushima N, Ohsumi Y, Uchiyama Y, et al. Impairment of starvation-induced and constitutive autophagy in Atg7-deficient mice. J Cell Biol 2005; 169:425-34; PMID:15866887; http://dx.doi.org/10.1083/jcb.200412022
  • Lecureuil C, Fontaine I, Crepieux P, Guillou F. Sertoli and granulosa cell-specific Cre recombinase activity in transgenic mice. Genesis 2002; 33:114-8; PMID:12124943; http://dx.doi.org/10.1002/gene.10100
  • Klionsky DJ, Abdelmohsen K, Abe A, Abedin MJ, Abeliovich H, Acevedo Arozena A, Adachi H, Adams CM, Adams PD, Adeli K, et al. Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition). Autophagy 2016; 12:1-222; PMID:26799652; http://dx.doi.org/10.1080/15548627.2015.1100356
  • Mundlos S, Pelletier J, Darveau A, Bachmann M, Winterpacht A, Zabel B. Nuclear localization of the protein encoded by the Wilms' tumor gene WT1 in embryonic and adult tissues. Development 1993; 119:1329-41; PMID:8306891
  • Kim KS, Cha MC, Gerton GL. Mouse sperm protein sp56 is a component of the acrosomal matrix. Biol Reprod 2001; 64:36-43; PMID:11133656; http://dx.doi.org/10.1095/biolreprod64.1.36
  • Goodson SG, Zhang Z, Tsuruta JK, Wang W, O'Brien DA. Classification of mouse sperm motility patterns using an automated multiclass support vector machines model. Biol Reprod 2011; 84:1207-15; PMID:21349820; http://dx.doi.org/10.1095/biolreprod.110.088989
  • Costoya JA, Hobbs RM, Barna M, Cattoretti G, Manova K, Sukhwani M, Orwig KE, Wolgemuth DJ, Pandolfi PP. Essential role of Plzf in maintenance of spermatogonial stem cells. Nat Genet 2004; 36:653-9; PMID:15156143; http://dx.doi.org/10.1038/ng1367
  • Kierszenbaum AL, Tres LL. The acrosome-acroplaxome-manchette complex and the shaping of the spermatid head. Arch Histol Cytol 2004; 67:271-84; PMID:15700535; http://dx.doi.org/10.1679/aohc.67.271
  • Kierszenbaum AL, Rivkin E, Tres LL. Molecular biology of sperm head shaping. Soc Reprod Fertility Suppl 2007; 65:33-43; PMID:17644953
  • O'Donnell L, O'Bryan MK. Microtubules and spermatogenesis. Semin Cell Dev Biol 2014; 30:45-54; PMID:24440897; http://dx.doi.org/10.1016/j.semcdb.2014.01.003
  • Vogl AW, Grove BD, Lew GJ. Distribution of Actin in Sertoli-Cell Ectoplasmic Specializations and Associated Spermatids in the Ground-Squirrel Testis. Anatomical Record 1986; 215:331-41; PMID:3526980; http://dx.doi.org/10.1002/ar.1092150402
  • Vogl AW, Du M, Wang XY, Young JS. Novel clathrin/actin-based endocytic machinery associated with junction turnover in the seminiferous epithelium. Semin Cell Dev Biol 2014; 30:55-64; PMID:24280271; http://dx.doi.org/10.1016/j.semcdb.2013.11.002
  • Upadhyay RD, Kumar AV, Ganeshan M, Balasinor NH. Tubulobulbar complex: cytoskeletal remodeling to release spermatozoa. Reprod Biol Endocrinol 2012; 10:27; http://dx.doi.org/10.1186/1477-7827-10-27
  • Young JS, Guttman JA, Vaid KS, Vogl AW. Tubulobulbar complexes are intercellular podosome-like structures that internalize intact intercellular junctions during epithelial remodeling events in the rat testis. Biol Reprod 2009; 80:162-74; PMID:18799754; http://dx.doi.org/10.1095/biolreprod.108.070623
  • Monastyrska I, Rieter E, Klionsky DJ, Reggiori F. Multiple roles of the cytoskeleton in autophagy. Biol Rev Camb Philos Soc 2009; 84:431-48; PMID:19659885; http://dx.doi.org/10.1111/j.1469-185X.2009.00082.x
  • Mackeh R, Perdiz D, Lorin S, Codogno P, Pous C. Autophagy and microtubules - new story, old players. J Cell Sci 2013; 126:1071-80; PMID:23620510; http://dx.doi.org/10.1242/jcs.115626
  • Zhuo C, Ji Y, Chen Z, Kitazato K, Xiang Y, Zhong M, Wang Q, Pei Y, Ju H, Wang Y. - MEFs reveals a close relationship between F-actin and autophagy. Biochem Biophys Res Commun 2013; 437:482-8; PMID:23850690; http://dx.doi.org/10.1016/j.bbrc.2013.06.111
  • Vallenius T, Luukko K, Makela TP. CLP-36 PDZ-LIM protein associates with nonmuscle alpha-actinin-1 and alpha-actinin-4. J Biol Chem 2000; 275:11100-5; PMID:10753915; http://dx.doi.org/10.1074/jbc.275.15.11100
  • Szczygiel M, Kurpisz M. Teratozoospermia and its effect on male fertility potential. Andrologia 1999; 31:63-75; PMID:10097795; http://dx.doi.org/10.1111/j.1439-0272.1999.tb02848.x
  • Breitbart H, Cohen G, Rubinstein S. Role of actin cytoskeleton in mammalian sperm capacitation and the acrosome reaction. Reproduction 2005; 129:263-8; PMID:15749953; http://dx.doi.org/10.1530/rep.1.00269
  • Sun X, Kovacs T, Hu YJ, Yang WX. The role of actin and myosin during spermatogenesis. Mol Biol Rep 2011; 38:3993-4001; PMID:21107714; http://dx.doi.org/10.1007/s11033-010-0517-0
  • O'Donnell L, Stanton PG, Bartles JR, Robertson DM. Sertoli cell ectoplasmic specializations in the seminiferous epithelium of the testosterone-suppressed adult rat. Biol Reprod 2000; 63:99-108; PMID:10859247; http://dx.doi.org/10.1095/biolreprod63.1.99
  • Wolski KM, Mruk DD, Cameron DF. The Sertoli-spermatid junctional complex adhesion strength is affected in vitro by adjudin. J Androl 2006; 27:790-4; PMID:16809272; http://dx.doi.org/10.2164/jandrol.106.000422
  • Vogl AW, Pfeiffer DC, Mulholland D, Kimel G, Guttman J. Unique and multifunctional adhesion junctions in the testis: ectoplasmic specializations. Arch Histol Cytol 2000; 63:1-15; PMID:10770585; http://dx.doi.org/10.1679/aohc.63.1
  • Lie PP, Mruk DD, Lee WM, Cheng CY. Cytoskeletal dynamics and spermatogenesis. Philos Trans R Soc Lond B Biol Sci 2010; 365:1581-92; PMID:20403871; http://dx.doi.org/10.1098/rstb.2009.0261
  • Chemes H. The phagocytic function of Sertoli cells: a morphological, biochemical, and endocrinological study of lysosomes and acid phosphatase localization in the rat testis. Endocrinology 1986; 119:1673-81; PMID:3757907; http://dx.doi.org/10.1210/endo-119-4-1673
  • Corcelle E, Nebout M, Bekri S, Gauthier N, Hofman P, Poujeol P, Fenichel P, Mograbi B. Disruption of autophagy at the maturation step by the carcinogen lindane is associated with the sustained mitogen-activated protein kinase/extracellular signal-regulated kinase activity. Cancer Res 2006; 66:6861-70; PMID:16818664; http://dx.doi.org/10.1158/0008-5472.CAN-05-3557
  • Nagda G, Bhatt DK. Alleviation of lindane induced toxicity in testis of Swiss mice (Mus musculus) by combined treatment with vitamin C, vitamin E and alpha-lipoic acid. Indian J Exp Biol 2011; 49:191-9; PMID:21452598
  • Bauer K, Kratzer M, Otte M, de Quintana KL, Hagmann J, Arnold GJ, Eckerskorn C, Lottspeich F, Siess W. Human CLP36, a PDZ-domain and LIM-domain protein, binds to alpha-actinin-1 and associates with actin filaments and stress fibers in activated platelets and endothelial cells. Blood 2000; 96:4236-45; PMID:11110697
  • Hasegawa T, Ohno K, Funahashi S, Miyazaki K, Nagano A, Sato K. CLP36 interacts with palladin in dorsal root ganglion neurons. Neurosci Lett 2010; 476:53-7; PMID:20381583; http://dx.doi.org/10.1016/j.neulet.2010.03.081
  • Grooman B, Fujiwara I, Otey C, Upadhyaya A. Morphology and viscoelasticity of actin networks formed with the mutually interacting crosslinkers: palladin and alpha-actinin. PloS one 2012; 7:e42773; PMID:22916157; http://dx.doi.org/10.1371/journal.pone.0042773
  • Ulbricht A, Gehlert S, Leciejewski B, Schiffer T, Bloch W, Hohfeld J. Induction and adaptation of chaperone-assisted selective autophagy CASA in response to resistance exercise in human skeletal muscle. Autophagy 2015; 11:538-46; PMID:25714469; http://dx.doi.org/10.1080/15548627.2015.1017186
  • Ridley AJ, Hall A. The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell 1992; 70:389-99; PMID:1643657; http://dx.doi.org/10.1016/0092-8674(92)90163-7
  • van der Wee KS, Johnson EW, Dirami G, Dym TM, Hofmann MC. Immunomagnetic isolation and long-term culture of mouse type A spermatogonia. J Androl 2001; 22:696-704; PMID:11451367
  • Jimenez T, Sanchez G, Wertheimer E, Blanco G. Activity of the Na,K-ATPase alpha 4 isoform is important for membrane potential, intracellular Ca2+, and pH to maintain motility in rat spermatozoa. Reproduction 2010; 139:835-45; PMID:20179187; http://dx.doi.org/10.1530/REP-09-0495
  • Song ZH, Yu HY, Wang P, Mao GK, Liu WX, Li MN, Wang HN, Shang YL, Liu C, Xu ZL, et al. Germ cell-specific Atg7 knockout results in primary ovarian insufficiency in female mice. Cell Death Dis 2015; 6:e1589; PMID:25590799; http://dx.doi.org/10.1038/cddis.2014.559

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.