Ehd4 is required to attain normal prepubertal testis size but dispensable for fertility in male mice

Genesis

Volumn 48, Issue 5, 2010, Pages 328-342

  George, Manju ^a   Rainey, Mark A ^a   Naramura, Mayumi ^a   Ying, GuoGuang ^b   Harms, Don W ^c   Vitaterna, Martha H ^d   Doglio, Lynn ^e   Crawford, Susan E ^e   Hess, Rex A ^f   Band, Vimla ^a,c   Band, Hamid ^a,c  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^b TIANJIN MEDICAL UNIVERSITY   (China)

^c UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^d NORTHWESTERN UNIVERSITY   (United States)

^e NORTHWESTERN UNIVERSITY   (United States)

^f UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

Compensation; EHD proteins; Endocytic recycling; Functional redundancy; Testis spermatogenesis

Indexed keywords

EH DOMAIN CONTAINING PROTEIN 4; GENOMIC DNA; MEMBRANE PROTEIN; UNCLASSIFIED DRUG;

ADULTHOOD; AGE DISTRIBUTION; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL COUNT; CELL PROLIFERATION; CONTROLLED STUDY; DEVELOPMENTAL GENE; DEVELOPMENTAL GENETICS; GENE DELETION; GENE FUNCTION; GERM CELL; KNOCKOUT GENE; MALE; MALE FERTILITY; MALE SUBFERTILITY; MOUSE; NONHUMAN; PERINATAL PERIOD; PREPUBERTY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEMINIFEROUS TUBULE; SEMINIFEROUS TUBULE EPITHELIUM; SERTOLI CELL; SPERMATID; SPERMATOCYTE; SPERMATOZOON COUNT; TESTIS DEVELOPMENT; TESTIS SIZE; TESTIS WEIGHT;

ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CELL PROLIFERATION; DNA-BINDING PROTEINS; FEMALE; FERTILITY; IMMUNOHISTOCHEMISTRY; IN SITU NICK-END LABELING; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED STRAINS; MICE, KNOCKOUT; NUCLEAR PROTEINS; ORGAN SIZE; SPERM COUNT; SPERM MOTILITY; SPERMATIDS; TESTIS; TIME FACTORS;

MUS;

EID: 77952046067     PISSN: 1526954X     EISSN: 1526968X     Source Type: Journal    
DOI: 10.1002/dvg.20620     Document Type: Article

References (33)

1. Bellve AR, Cavicchia JC, Millette CF, O'Brien DA, Bhatnagar YM, Dym M. 1977. Spermatogenic cells of the prepuberal mouse: Isolation and morphological characterization. J Cell Biol 74:68-85. (Pubitemid 8141486)
2. Blume JJ, Halbach A, Behrendt D, Paulsson M, Plomann M. 2007. EHD proteins are associated with tubular and vesicular compartments and interact with specific phospholipids. Exp Cell Res 313:219-231. (Pubitemid 46048812)
3. Bonanomi D, Fornasiero EF, Valdez G, Halegoua S, Benfonati F, Menegon A, Valtorta F. 2008. Identification of a developmentally regulated pathway of membrane retrieval in neuronal growth cones. J Cell Sci 121:3757-3769.
4. Braun A, Pinyol R, Dahlhaus R, Koch D, Fonarev P, Grant BD, Kessels MM, Qualmann B. 2005. EHD proteins associate with syndapin I and II and such interactions play a crucial role in endosomal recycling. Mol Biol Cell 16:3642-3658. (Pubitemid 41078817)
5. Chapman DL, Wolgemuth DJ. 1994. Expression of proliferating cell nuclear antigen in the mouse germ line and surrounding somatic cells suggests both proliferation-dependent and -independent modes of function. Int J Dev Biol 38:491-497.
6. Clermont Y. 1972. Kinetics of spermatogenesis in mammals: Seminiferous epithelium cycle and spermatogonial renewal. Physiol Rev 52:198-236.
7. Daumke O, Lundmark R, Vallis Y, Martens S, Butler PJ, McMahon HT. 2007. Architectural and mechanistic insights into an EHD ATPase involved in membrane remodelling. Nature 449:923-927. (Pubitemid 47598607)
8. Doherty KR, Demonbreun AR, Wallace GQ, Cave A, Posey AD, Heretis K, Pytel P, McNally EM. 2008. The endocytic recycling protein EHD2 interacts with myoferlin to regulate myoblast fusion. J Biol Chem 283:20252-20260.
9. George M, Ying G, Rainey MA, Solomon A, Parikh PT, Gao Q, Band V, Band H. 2007. Shared as well as distinct roles of EHD proteins revealed by biochemical and functional comparisons in mammalian cells and C. elegans. BMC Cell Biol 8:3. (Pubitemid 46231619)
10. Grant BD, Caplan S. 2008. Mechanisms of EHD/RME-1 protein function in endocytic transport. Traffic 12:2043-2052.
11. Guilherme A, Soriano NA, Furcinitti PS, Czech MP. 2004. Role of EHD1 and EHBP1 in perinuclear sorting and insulin-regulated GLUT4 recycling in 3T3-L1 adipocytes. J Biol Chem 279:40062-40075. (Pubitemid 39258281)
12. He Z, Jiang J, Hofmann MC, Dym M. 2007. Gfra1 silencing in mouse spermatogonial stem cells results in their differentiation via the inactivation of RET tyrosine kinase. Biol Reprod 77:723-733. (Pubitemid 47494388)
13. Jovic M, Naslavsky N, Rapaport D, Horowitz M, Caplan S. 2007. EHD1 regulates beta1 integrin endosomal transport: Effects on focal adhesions, cell spreading and migration. J Cell Sci 120: 802-814. (Pubitemid 46523482)
14. Kuo HJ, Tran NT, Clary SA, Morris NP, Glanville RW. 2001. Characterization of EHD4, an EH domain-containing protein expressed in the extracellular matrix. J Biol Chem 276:43103-43110. (Pubitemid 37370994)
15. Lee DW, Zhao X, Scarselletta S, Schweinsberg PJ, Eisenberg E, Grant BD, Greene LE. 2005. ATP binding regulates oligomerization and endosome association of RME-1 family proteins. J Biol Chem 280:17213-17220. (Pubitemid 41389188)
16. Lee J, Richburg JH, Younkin SC, Boekelheide K. 1997. The fas system is a key regulator of germ cell apoptosis in the testis. Endocrinology 138:2081-2088. (Pubitemid 27180828)
17. Liu P, Jenkins NA, Copeland NG. 2003. A highly efficient recombineering-based method for generating conditional knockout mutations. Genome Res 13:476-484. (Pubitemid 36395405)
18. Lizama C, Alfaro I, Reyes JG, Moreno RD. 2007. Up-regulation of CD95 (apo-1/Fas) is associated with spermatocyte apoptosis during the first round of spermatogenesis in the rat. Apoptosis 12:499-512. (Pubitemid 46318903)
19. Maxfield FR, McGraw TE. 2004. Endocytic recycling. Nat Rev Mol Cell Biol 5:121-132.
20. Meng X, Lindahl M, Hyvonen ME, Parvinen M, de Rooij DG, Hess MW, Raatikainen-Ahokas A, Sainio K, Rauvala H, Lakso M, Pichel JG, Westphal H, Saarma M, Sariola H. 2000. Regulation of cell fate decision of undifferentiated spermatogonia by GDNF. Science 287:1489-1493. (Pubitemid 30127143)
21. Naslavsky N, McKenzie J, Altan-Bonnet N, Sheff D, Caplan S. 2009. EHD3 regulates early-endosome-to-golgi transport and preserves golgi morphology. J Cell Sci 122:389-400.
22. Naslavsky N, Rahajeng J, Chenavas S, Sorgen PL, Caplan S. 2007a. EHD1 and Eps15 interact with phosphatidylinositols via their Eps15 homology domains. J Biol Chem 282:16612-16622. (Pubitemid 47100376)
23. Naslavsky N, Rahajeng J, Rapaport D, Horowitz M, Caplan S. 2007b. EHD1 regulates cholesterol homeostasis and lipid droplet storage. Biochem Biophys Res Commun 357:792-799. (Pubitemid 46653849)
24. Naslavsky N, Rahajeng J, Sharma M, Jovic M, Caplan S. 2006. Interactions between EHD proteins and Rab11-FIP2: A role for EHD3 in early endosomal transport. Mol Biol Cell 17:163-177. (Pubitemid 43049471)
25. Print CG, Loveland KL. 2000. Germ cell suicide: New insights into apoptosis during spermatogenesis. Bioessays 22:423-430.
26. Rainey MA, George M, Ying GG, Akakura R, Burgess DJ, Siefker E, Bargar T, Doglio L, Crawford SE, Todd GL, Govindarajan V, Hess RA, Band V, Naramura M, Band H. 2010. The endocytic recycling regulator EHD1 is essential for spermatogenesis and male fertility in mice. BMC Dev Biol in press.
27. Rapaport D, Auerbach W, Naslavsky N, Pasmanik-Chor M, Galperin E, Fein A, Caplan S, Joyner AL, Horowitz M. 2006. Recycling to the plasma membrane is delayed in EHD1 knockout mice. Traffic 7:52-60.
28. Rodriguez I, Ody C, Araki K, Garcia I, Vassalli P. 1997. An early and massive wave of germinal cell apoptosis is required for the development of functional spermatogenesis. EMBO J 16:2262-2270. (Pubitemid 27260376)
29. Sengupta S, George M, Miller KK, Naik K, Chou J, Cheatham MA, Dallos P, Naramura M, Band H, Zheng J. 2009. EHD4 and CDH23 are interacting partners in cochlear hair cells. J Biol Chem 284:20121-20129.
30. Shao Y, Akmentin W, Toledo-Aral JJ, Rosenbaum J, Valdez G, Cabot JB, Hilbush BS, Halegoua S. 2002. Pincher, a pinocytic chaperone for nerve growth factor/TrkA signaling endosomes. J Cell Biol 157: 679-691. (Pubitemid 34839795)
31. Sharma M, Naslavsky N, Caplan S. 2008. A role for EHD4 in the regulation of early endosomal transport. Traffic 9:995-1018. (Pubitemid 351639501)
32. Valdez G, Akmentin W, Philippidou P, Kuruvilla R, Ginty DD, Halegoua S. 2005. Pincher-mediated macroendocytosis underlies retrograde signaling by neurotrophin receptors. J Neurosci 25:5236-5247. (Pubitemid 40726976)
33. Wang RA, Nakane PK, Koji T. 1998. Autonomous cell death of mouse male germ cells during fetal and postnatal period. Biol Reprod 58:1250-1256. (Pubitemid 28217250)