CoChat
Sign Up
Cited by 65

The DOI matches its Crossref record; 1 of the 1 references it cites were found in a registry or an index.

The endocytic recycling regulator EHD1 is essential for spermatogenesis and male fertility in mice

Rainey, Mark A, George, Manju, Ying, GuoGuang, Akakura, Reiko, Burgess, Daniel J, Siefker, Ed, Bargar, Tom, Doglio, Lynn, Crawford, Susan E, Todd, Gordon L, Govindarajan, Venkatesh, Hess, Rex A, Band, Vimla, Naramura, Mayumi, Band, Hamid·2010·BMC Developmental Biology
DOI 10.1186/1471-213x-10-37PMC PMC2856533
Open this paper in CoChat — free account

Abstract

Background: The C-terminal Eps15 homology domain-containing protein 1 (EHD1) is ubiquitously expressed and regulates the endocytic trafficking and recycling of membrane components and several transmembrane receptors. To elucidate the function of EHD1 in mammalian development, we generated Ehd1 -/- mice using a Cre/ loxP system. Results: Both male and female Ehd1 -/- mice survived at sub-Mendelian ratios. A proportion of Ehd1 -/- mice were viable and showed smaller size at birth, which continued into adulthood. Ehd1 -/- adult males were infertile and displayed decreased testis size, whereas Ehd1 -/- females were fertile. In situ hybridization and immunohistochemistry of developing wildtype mouse testes revealed EHD1 expression in most cells of the seminiferous epithelia. Histopathology revealed abnormal spermatogenesis in the seminiferous tubules and the absence of mature spermatozoa in the epididymides of Ehd1 -/- males. Seminiferous tubules showed disruption of the normal spermatogenic cycle with abnormal acrosomal development on round spermatids, clumping of acrosomes, misaligned spermatids and the absence of normal elongated spermatids in Ehd1 -/- males. Light and electron microscopy analyses indicated that elongated spermatids were abnormally phagocytosed by Sertoli cells in Ehd1 -/- mice. Conclusions: Contrary to a previous report, these results demonstrate an important role for EHD1 in pre- and post-natal development with a specific role in spermatogenesis.

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1186/1471-213x-10-37

Cites

1 of 1 references verified0 citation errors · 0 not checkable

Statistics

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

Cites

Flagged first, then by citations

Research works printed but not linked: 42

  1. Naslavsky N, Caplan S: C-terminal EH-domain-containing proteins: consensus for a role in endocytic trafficking, EH?. J Cell Sci. 2005, 118 (Pt 18): 4093-4101. 10.1242/jcs.02595. · DOI · Paper page
  2. Grant B, Zhang Y, Paupard MC, Lin SX, Hall DH, Hirsh D: Evidence that RME-1, a conserved C. elegans EH-domain protein, functions in endocytic recycling. Nat Cell Biol. 2001, 3 (6): 573-579. 10.1038/35078549. · DOI
  3. Olswang-Kutz Y, Gertel Y, Benjamin S, Sela O, Pekar O, Arama E, Steller H, Horowitz M, Segal D: Drosophila Past1 is involved in endocytosis and is required for germline development and survival of the adult fly. J Cell Sci. 2009, 122 (Pt 4): 471-480. 10.1242/jcs.038521. · DOI
  4. Lee DW, Zhao X, Scarselletta S, Schweinsberg PJ, Eisenberg E, Grant BD, Greene LE: ATP binding regulates oligomerization and endosome association of RME-1 family proteins. J Biol Chem. 2005, 280 (17): 17213-17220. 10.1074/jbc.M412751200. · DOI
  5. Daumke O, Lundmark R, Vallis Y, Martens S, Butler PJ, McMahon HT: Architectural and mechanistic insights into an EHD ATPase involved in membrane remodelling. Nature. 2007, 449 (7164): 923-927. 10.1038/nature06173. · DOI · Paper page
  6. George M, Ying G, Rainey MA, Solomon A, Parikh PT, Gao Q, Band V, Band H: Shared as well as distinct roles of EHD proteins revealed by biochemical and functional comparisons in mammalian cells and C. elegans. BMC Cell Biol. 2007, 8: 3-10.1186/1471-2121-8-3. · DOI · Paper page
  7. Sharma M, Naslavsky N, Caplan S: A role for EHD4 in the regulation of early endosomal transport. Traffic. 2008, 9 (6): 995-1018. 10.1111/j.1600-0854.2008.00732.x. · DOI · Paper page
  8. Mintz L, Galperin E, Pasmanik-Chor M, Tulzinsky S, Bromberg Y, Kozak CA, Joyner A, Fein A, Horowitz M: EHD1--an EH-domain-containing protein with a specific expression pattern. Genomics. 1999, 59 (1): 66-76. 10.1006/geno.1999.5800. · DOI · Paper page
  9. Salcini AE, Confalonieri S, Doria M, Santolini E, Tassi E, Minenkova O, Cesareni G, Pelicci PG, Di Fiore PP: Binding specificity and in vivo targets of the EH domain, a novel protein-protein interaction module. Genes Dev. 1997, 11 (17): 2239-2249. 10.1101/gad.11.17.2239. · DOI · Paper page
  10. Mellman I: Endocytosis and molecular sorting. Annu Rev Cell Dev Biol. 1996, 12: 575-625. 10.1146/annurev.cellbio.12.1.575. · DOI
  11. Maxfield FR, McGraw TE: Endocytic recycling. Nat Rev Mol Cell Biol. 2004, 5 (2): 121-132. 10.1038/nrm1315. · DOI · Paper page
  12. Soldati T, Schliwa M: Powering membrane traffic in endocytosis and recycling. Nat Rev Mol Cell Biol. 2006, 7 (12): 897-908. 10.1038/nrm2060. · DOI
  13. Grant BD, Caplan S: Mechanisms of EHD/RME-1 protein function in endocytic transport. Traffic. 2008, 9 (12): 2043-2052. 10.1111/j.1600-0854.2008.00834.x. · DOI
  14. Lin SX, Grant B, Hirsh D, Maxfield FR: Rme-1 regulates the distribution and function of the endocytic recycling compartment in mammalian cells. Nat Cell Biol. 2001, 3 (6): 567-572. 10.1038/35078543. · DOI · Paper page
  15. Jovic M, Naslavsky N, Rapaport D, Horowitz M, Caplan S: EHD1 regulates beta1 integrin endosomal transport: effects on focal adhesions, cell spreading and migration. J Cell Sci. 2007, 120 (Pt 5): 802-814. 10.1242/jcs.03383. · DOI
  16. Caplan S, Naslavsky N, Hartnell LM, Lodge R, Polishchuk RS, Donaldson JG, Bonifacino JS: A tubular EHD1-containing compartment involved in the recycling of major histocompatibility complex class I molecules to the plasma membrane. EMBO J. 2002, 21 (11): 2557-2567. 10.1093/emboj/21.11.2557. · DOI
  17. Naslavsky N, Boehm M, Backlund PS, Caplan S: Rabenosyn-5 and EHD1 interact and sequentially regulate protein recycling to the plasma membrane. Mol Biol Cell. 2004, 15 (5): 2410-2422. 10.1091/mbc.E03-10-0733. · DOI
  18. Guilherme A, Soriano NA, Furcinitti PS, Czech MP: Role of EHD1 and EHBP1 in perinuclear sorting and insulin-regulated GLUT4 recycling in 3T3-L1 adipocytes. J Biol Chem. 2004, 279 (38): 40062-40075. 10.1074/jbc.M401918200. · DOI
  19. Gokool S, Tattersall D, Seaman MN: EHD1 interacts with retromer to stabilize SNX1 tubules and facilitate endosome-to-Golgi retrieval. Traffic. 2007, 8 (12): 1873-1886. 10.1111/j.1600-0854.2007.00652.x. · DOI · Paper page
  20. Valdez G, Akmentin W, Philippidou P, Kuruvilla R, Ginty DD, Halegoua S: Pincher-mediated macroendocytosis underlies retrograde signaling by neurotrophin receptors. J Neurosci. 2005, 25 (21): 5236-5247. 10.1523/JNEUROSCI.5104-04.2005. · DOI · Paper page
  21. Naslavsky N, Rahajeng J, Sharma M, Jovic M, Caplan S: Interactions between EHD proteins and Rab11-FIP2: a role for EHD3 in early endosomal transport. Mol Biol Cell. 2006, 17 (1): 163-177. 10.1091/mbc.E05-05-0466. · DOI · Paper page
  22. Naslavsky N, McKenzie J, Altan-Bonnet N, Sheff D, Caplan S: EHD3 regulates early-endosome-to-Golgi transport and preserves Golgi morphology. J Cell Sci. 2009, 122 (Pt 3): 389-400. 10.1242/jcs.037051. · DOI
  23. Guilherme A, Soriano NA, Bose S, Holik J, Bose A, Pomerleau DP, Furcinitti P, Leszyk J, Corvera S, Czech MP: EHD2 and the novel EH domain binding protein EHBP1 couple endocytosis to the actin cytoskeleton. J Biol Chem. 2004, 279 (11): 10593-10605. 10.1074/jbc.M307702200. · DOI · Paper page
  24. Doherty KR, Demonbreun AR, Wallace GQ, Cave A, Posey AD, Heretis K, Pytel P, McNally EM: The endocytic recycling protein EHD2 interacts with myoferlin to regulate myoblast fusion. J Biol Chem. 2008, 283 (29): 20252-20260. 10.1074/jbc.M802306200. · DOI
  25. Gatti JL, Metayer S, Belghazi M, Dacheux F, Dacheux JL: Identification, proteomic profiling, and origin of ram epididymal fluid exosome-like vesicles. Biol Reprod. 2005, 72 (6): 1452-1465. 10.1095/biolreprod.104.036426. · DOI
  26. Rapaport D, Auerbach W, Naslavsky N, Pasmanik-Chor M, Galperin E, Fein A, Caplan S, Joyner AL, Horowitz M: Recycling to the plasma membrane is delayed in EHD1 knockout mice. Traffic. 2006, 7 (1): 52-60. 10.1111/j.1600-0854.2005.00359.x. · DOI · Paper page
  27. Russell LD, Ettlin RA, Hikim AP, Clegg ED: Histological and Histopathological Evaluation of the Testis. 1990, St. Louis, MO: Cache River Press
  28. Ahmed EA, de Rooij DG: Staging of mouse seminiferous tubule cross- sections. Methods Mol Biol. 2009, 558: 263-277. full_text. · DOI
  29. Mori C, Nakamura N, Dix DJ, Fujioka M, Nakagawa S, Shiota K, Eddy EM: Morphological analysis of germ cell apoptosis during postnatal testis development in normal and Hsp 70-2 knockout mice. Dev Dyn. 1997, 208 (1): 125-136. 10.1002/(SICI)1097-0177(199701)208:1<125::AID-AJA12>3.0.CO;2-5. · DOI
  30. Yan HH, Mruk DD, Lee WM, Cheng CY: Blood-testis barrier dynamics are regulated by testosterone and cytokines via their differential effects on the kinetics of protein endocytosis and recycling in Sertoli cells. FASEB J. 2008, 22 (6): 1945-1959. 10.1096/fj.06-070342. · DOI
  31. Russell L: Observations on rat Sertoli ectoplasmic ('junctional') specializations in their association with germ cells of the rat testis. Tissue Cell. 1977, 9 (3): 475-498. 10.1016/0040-8166(77)90007-6. · DOI
  32. 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?. Hum Reprod Update. 2004, 10 (4): 349-369. 10.1093/humupd/dmh026. · DOI
  33. Mruk DD, Cheng CY: Sertoli-Sertoli and Sertoli-germ cell interactions and their significance in germ cell movement in the seminiferous epithelium during spermatogenesis. Endocr Rev. 2004, 25 (5): 747-806. 10.1210/er.2003-0022. · DOI
  34. Yan HH, Mruk DD, Cheng CY: Junction restructuring and spermatogenesis: the biology, regulation, and implication in male contraceptive development. Curr Top Dev Biol. 2008, 80: 57-92. full_text. · DOI
  35. Xia W, Wong EW, Mruk DD, Cheng CY: TGF-beta3 and TNFalpha perturb blood-testis barrier (BTB) dynamics by accelerating the clathrin-mediated endocytosis of integral membrane proteins: a new concept of BTB regulation during spermatogenesis. Dev Biol. 2009, 327 (1): 48-61. 10.1016/j.ydbio.2008.11.028. · DOI
  36. Li MW, Xia W, Mruk DD, Wang CQ, Yan HH, Siu MK, Lui WY, Lee WM, Cheng CY: Tumor necrosis factor {alpha} reversibly disrupts the blood-testis barrier and impairs Sertoli-germ cell adhesion in the seminiferous epithelium of adult rat testes. J Endocrinol. 2006, 190 (2): 313-329. 10.1677/joe.1.06781. · DOI
  37. Sarkar O, Mathur PP, Cheng CY, Mruk DD: Interleukin 1 alpha (IL1A) is a novel regulator of the blood-testis barrier in the rat. Biol Reprod. 2008, 78 (3): 445-454. 10.1095/biolreprod.107.064501. · DOI
  38. Mayer H, Bilban M, Kurtev V, Gruber F, Wagner O, Binder BR, de Martin R: Deciphering regulatory patterns of inflammatory gene expression from interleukin-1-stimulated human endothelial cells. Arterioscler Thromb Vasc Biol. 2004, 24 (7): 1192-1198. 10.1161/01.ATV.0000131263.06296.77. · DOI
  39. Tegelenbosch RA, de Rooij DG: A quantitative study of spermatogonial multiplication and stem cell renewal in the C3H/101 F1 hybrid mouse. Mutat Res. 1993, 290 (2): 193-200. · DOI
  40. Liu P, Jenkins NA, Copeland NG: A highly efficient recombineering-based method for generating conditional knockout mutations. Genome Res. 2003, 13 (3): 476-484. 10.1101/gr.749203. · DOI
  41. Andoniou CE, Lill NL, Thien CB, Lupher ML, Ota S, Bowtell DD, Scaife RM, Langdon WY, Band H: The Cbl proto-oncogene product negatively regulates the Src-family tyrosine kinase Fyn by enhancing its degradation. Mol Cell Biol. 2000, 20 (3): 851-867. 10.1128/MCB.20.3.851-867.2000. · DOI
  42. Govindarajan V, Ito M, Makarenkova HP, Lang RA, Overbeek PA: Endogenous and ectopic gland induction by FGF-10. Dev Biol. 2000, 225 (1): 188-200. 10.1006/dbio.2000.9812. · DOI

Cited by

Sorted by citations

Metadata

Authors
Rainey, M. A., George, M., Ying, G., Akakura, R., Burgess, D. J., Siefker, E., Bargar, T., Doglio, L., Crawford, S. E., Todd, G. L., Govindarajan, V., Hess, R. A., Band, V., Naramura, M., & Band, H.
Venue
BMC Developmental Biology
Publisher
Springer Science and Business Media LLC
Published
2010-04-02
Volume
10
Issue
1
ISSN
1471-213X
DOI
10.1186/1471-213x-10-37
PMC
PMC2856533
Cited by
65
References
1
Language
en

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review