Cell and Tissue Biology

, Volume 6, Issue 3, pp 254–267 | Cite as

The role of chromatoid bodies and cytoskeleton in differentiation of rat spermatozoids

  • E. S. Snigirevskaya
  • M. I. Mosevitsky
  • Ya. Yu. Komissarchik


An ultrastructural and immunocytochemical study of rat male germ cells at different stages of development has been carried out. Investigation of morphological changes of spermatogenic cells showed the presence of close associations between chromatoid bodies (CBs) and other cell organelles, particularly with the nucleus and Golgi apparatus. In addition, a connection of manchette noncentosomal microtubules (MTs) with spermatid perinuclear ring plasma membrane (PM) in the zone of adhesion intercellular contact, zonula adhaerens (ZA), was revealed. These results, as well as the available literary data, make it possible to analyze expected pathways of noncentrosomal MT nucleation in the late spermatids. It is possible to suggest that noncentorosomal MT are nucleated on the sites of perinuclear ring ZA. The immunocytochemical analysis revealed two novel proteins for these cells: BASP1 and MARCKS. It was shown that these proteins were present in CBs in early spermatids. During spermatozoid differentiation, these proteins are located along the outer dense fibers (ODFs) of the sperm tail. BASP1 and MARCKS are believed to be involved in the processes of calcium accumulation in CBs and ODFs. Calcium ions seem to play a significant role in RNA processing and protein synthesis in spermatids. Calcium is also necessary for sperm mobility defined mainly by ODFs.


rat spermatogenesis chromatoid body outer dense fibers microtubules manchette BASP1 MARCKS 



Golgi apparatus




outer dense fiber


intermediate junction


plasma membrane


chromatoid body


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  1. Andonov, M., Further Study of the Chromatoid Body in Rat Spermatocytes and Spermatids, Z Mikrosk. Anat. Forsch., 1990, vol. 104, pp. 46–54.PubMedGoogle Scholar
  2. Andonov, M.D. and Chaldakov, G.N., Role of Ca2+ and cAMP in Rat Spermatogenesis-Ultrastructural Evidences, Acta Histochem. Suppl., 1991, vol. 41, pp. 55–63.PubMedGoogle Scholar
  3. Anton, E., Association of Golgi Vesicles Containing acid Phosphatase with the Chromatoid Body of Rat Spermatids, Experientia, 1983, vol. 39, pp. 393–394.PubMedCrossRefGoogle Scholar
  4. Bagchi, M., Kousis, S., and Maisel, H., BASP1 in the Lens, J. Cell Biochem., 2008, vol. 105, pp. 699–702.PubMedCrossRefGoogle Scholar
  5. Baltz, J.M., Williams, P.O., and Cone, R.A., Dense Fibers Protect Mammalian Sperm against Damage, Biol. Reproduct., 1990, vol. 43, pp. 485–491.CrossRefGoogle Scholar
  6. Beach, S.F. and Vogl, A.W., Spermatid Translocation in the Rat Seminiferous Epithelium: Coupling Membrane Trafficking Machinery to a Junction Plaque, Biol. Reproduct., 1999, vol. 60, pp. 1036–1046.CrossRefGoogle Scholar
  7. Biggiogera, M., Fakan, S., Leser, G., Martin, T.E., and Gordon, J., Immunoelectron Microscopical Visualization of Ribonucleoproteins in the Chromatoid Body of Mouse Spermatids, Mol. Reprod. Develop., 1990, vol. 26, pp. 150–158.CrossRefGoogle Scholar
  8. Brostrom, M.A., and Brostrom, C.O., Calcium Dynamics and Endoplasmic Reticular Function in the Regulation of Protein Synthesis: Implications for Cell Growth and Adaptability, Cell Calcium, 2003, vol. 34, pp. 345–63.PubMedCrossRefGoogle Scholar
  9. Carpenter, K.J., Hill, K.J., Charalambous, M., Wagner, K.J., Lahiri, D., and James, D.I., BASP1 Is a Transcriptional Cosuppressor for the Wilms’ Tumor Suppressor Protein WT1, Mol. Cell Biol., 2004, vol. 24, pp. 537–549.PubMedCrossRefGoogle Scholar
  10. Chabin-Brion, K., Marceiller, J., Perez, F., Drechou, A., Durand, G., and Pous, C., The Golgi Complex Is a Microtubule-Organizing Organelle, Mol. Biol. Cell., 2001, vol. 12, pp. 2047–2060.PubMedGoogle Scholar
  11. Chakravarthy, B., Morley, P., and Whitfield, J., Ca2+-Calmodulin and Protein Kinase Cs: A Hypothetical Synthesis of Their Conflicting Convergences on Shared Substrate Domains, Trends Neurosci., 1999, vol. 22, pp. 12–16.PubMedCrossRefGoogle Scholar
  12. Chuma, S., Hosokawa, M., Tanaka, T., and Nakatsuji, N., Ultrastructural Characterization of Spermatogenesis and Its Evolutionary Conservation in the Germline: Germinal Granules in Mammals, Mol. Cell Endocrinol., 2009, vol. 306, pp. 17–23.PubMedCrossRefGoogle Scholar
  13. Cole, A., Meistrich, M.L., Cherry, L.M., and TrestleWeige, P.K., Nuclear and Manchette Development in Spermatids of Normal and azh/azh Mutant Mice, Biol. Reprod., 1988, vol. 38, pp. 385–401.PubMedCrossRefGoogle Scholar
  14. Drozdov, A.L. and Ivankov, V.N., Morfologiya gamet zhivotnykh (Morphology of Animal Gametes), Moscow: Izd. Dom Kruglyi God, 2000.Google Scholar
  15. Efimov, A., Kharitonov, A., Efimova, N., Loncarek, J., Miller, P.M., Andreyeva, N., Gleeson, P., Galjart, N., Maia, A.R., McLeod, I.X., Yates, J.R., III, Maiato, H., Khodjakov, A., Akhmanova, A., and Kaverina, I., Assymetric CLASP-Dependent Nucleation of Noncentrosomal Microtubules at the Trans-Golgi Network, Dev. Cell., 2007, vol. 12, pp. 917–930.PubMedCrossRefGoogle Scholar
  16. Fawcett, D.W., A Comparative View of Sperm Ultrastructure, Biol. Reproduct., 1970, vol. 2, pp. 90–127.CrossRefGoogle Scholar
  17. Fawcett, D.W., Anderson, W.A., and Phillips, D.M., Morphogenetic Factors Influencing the Shape of the Sperm Head, Dev. Boil., 1971, vol. 26, pp. 220–251.CrossRefGoogle Scholar
  18. Fawcett, D.W., Eddy, E.M., and Phillips, D.M., Observations of the fine Structure and Relationships of the Chromatoid Body in Mammalian Spermatogenesis, Biol. Reproduct., 1970, vol. 2, pp. 129–153.CrossRefGoogle Scholar
  19. Figueroa, J. and Burzio, L.O., Polysome-Like Structures in the Chromatoid Body of Rat Spermatids, Cell Tissue Res., 1998, vol. 291, pp. 575–579.PubMedCrossRefGoogle Scholar
  20. Fouquet, J.-P., Kann, M.L., Combeau, C., and Melki, R., β-Tubulin during the Differentiation of Spermatozoa in Various Mammals and Man, Mol. Human Reproduct., 1998, vol. 4, pp. 1122–1129.CrossRefGoogle Scholar
  21. Frey, D., Laux, T., Xu, L., Schneider, C., and Caroni, P., Shared and Unique Roles of CAP23 and GAP43 in Actin Regulation, Neurite Outgrowth, and Anatomical Plasticity, J. Cell Biol., 2000, vol. 149, pp. 1443–1454.PubMedCrossRefGoogle Scholar
  22. Göb, E., Schmitt, J., Benavente, R., and Alsheimer, M., Mammalian Sperm Head Formation Involves Different Polarization of Two Novel LINC Complexes, PLoS One, 2010, vol. 5, p. e12072.Google Scholar
  23. Gilbert, S.F., Developmental Biology, 6th ed., Sunderland, Massachusetts: Sinauer Associates Inc., 2000.Google Scholar
  24. Gunawardana, V.K., and Scott, M.G.A.D., Ultrastructural Studies on the Differentiation of Spermatids in the Domestic Fowl, J. Anat., 1977, vol. 124, pp. 741–755.PubMedGoogle Scholar
  25. Haidl, G., Becker, A., and Henkel, R., Poor Development of Outer Dense Fibers as a Major Cause of Tail Abnormalities on the Spermatozoa of Asthenoteratozoospermic Men, Hum. Reprod., 1991, vol. 6, pp. 1431–1438.PubMedGoogle Scholar
  26. Ham, A. and Cormac, D., Gistologiya (Histology), Moscow: Mir, 1983, vol. 5.Google Scholar
  27. Hartl, M., Nist, A., Khan, M.I., Valovka, T., and Bister, K., Inhibition of Myc-Induced Cell Transformation by Brain Acid-Soluble Protein 1 (BASP1), Proc. Natl. Acad. Sci. USA, 2009, vol. 106, pp. 5604–5609.PubMedCrossRefGoogle Scholar
  28. Henkel, R., Stalf, T., Mertens, N., Miska, W., and Schill, W.-B., Outer Dense Fibres of Human Spermatozoa: Partial Characterization and Possible Physiological Functions, Int. J. Androl., 2009, vol. 17, pp. 68–73.CrossRefGoogle Scholar
  29. Kierszenbaum, A., Rivkin, E., Tres, L.L., Yoder, B.K., Haycraft, C.J., Bornens, M., and Rios, R.M., GMAP210 and IFT88 Are Present in the Spermatid Golgi Apparatus and Participate in the Development of the Acrosome-Acroplaxome Complex, Head-Tail Coupling Apparatus and Tail, Develop. Dynamics, 2011, vol. 240, pp. 723–736.CrossRefGoogle Scholar
  30. Kierszenbaum, A.L. and Tres, L.L., The Acrosome-Acroplaxome-Manchette Complex and the Shaping of the Spermatid Head, Arch. Histol. Cytol., 2004, vol. 67, pp. 271–284.PubMedCrossRefGoogle Scholar
  31. Kierszenbaum, A.L. and Tres, L.L., The Acrosome-Acroplaxome-Manchette Complex and the Shaping of the Spermatid Head, Arch. Histol. Cytol., 2010, vol. 67, pp. 271–284.CrossRefGoogle Scholar
  32. Kierszenbaum, A.L., Intramanchette Transport (IMT): Managing the Making of the Spermatid Head, Centrosome, and Tail, Mol. Reprod. Dev., 2002, vol. 63, pp. 1–4.PubMedCrossRefGoogle Scholar
  33. Kierszenbaum, A.L., Rivkin, E., and Tres, L.L., Acroplaxome, an F-Actin-Keratin-Containing Plate, Anchors the Acrosome to the Nucleus during Shaping of the Spermatid Head, Mol. Biol. Cell, 2003, vol. 14, pp. 4628–4640.PubMedCrossRefGoogle Scholar
  34. Kierszenbaum, A.L., Spermatid Manchette: Plugging Proteins to Zero into the Sperm Tail, Mol. Reprod. Dev., 2001, vol. 59, pp. 347–349.PubMedCrossRefGoogle Scholar
  35. Kierszenbaum, A.L., Tres, L.L., Rivkin, E., Haycraft, C.J., and Yoder, B.K., Disrupted Intramanchette and Intraflagellar Cargo Transport in Spermatids of the orpk Mutant Mouse, Mol. Biol. Cell., 2004, vol. 15, p. 132a.Google Scholar
  36. Kim, Y.H., McFarlane, J.R., O’Bryan, M.K., Almahbobi, G., Temple-Smith, P.D., and de Kretser, D.M., Isolation and Characterization of Rat Sperm Tail Outer Dense Fibres and Comparison with Rabbit and Human Spermatozoa Using a Polyclonal Antiserum, J. Reprod. Fertil., 1999, vol. 116, pp. 345–353.PubMedCrossRefGoogle Scholar
  37. Kodani, A. and Sutterlin, C., A New Function for an Old Organelle: Microtubule Nucleation at the Golgi Apparatus, EMBO J., 2009, vol. 28, pp. 995–996.PubMedCrossRefGoogle Scholar
  38. Korshunova, I., Caroni, P., Kolkova, K., Berezin, V., Bock, E., and Walmod, P.S., Characterization of BASP1-Mediated Neurite Outgrowth, J. Neurosci. Res., 2008, vol. 86, pp. 2201–2213.PubMedCrossRefGoogle Scholar
  39. Kotaja, N., and Sassone-Corsi, P., The Chromatoid Body: A Germ-Cell-Specific RNA-Processing Centre, Nat. Rev. Mol. Cell Biol., 2007, vol. 8, pp. 85–90.PubMedCrossRefGoogle Scholar
  40. Kotaja, N., Lin, H., Parvinen, M., and Sassone-Corsi, P., Interplay of PIWI/Argonaute Protein MIWI and Kinesin KIF17b in Chromatoid Bodies of Male Germ Cells, J. Cell Sci., 2006, vol. 119, pp. 2819–2825.PubMedCrossRefGoogle Scholar
  41. Lee, N.P.Y., and Cheng, C.Y., Ectoplasmic Specialization, a Testis-Specific Cell-Cell Actin-Based Adherens Junction Type: Is this a Potential Target for Male Contraceptive Development? Human Reproduct., 2004, vol. 10, pp. 349–369.CrossRefGoogle Scholar
  42. Lie, P.P.Y., Mruk, D.D., Lee, W.M., and Cheng, C.Y., Cytoskeletal Dynamics and Spermatogenesis, Phil.Trans. R. Soc., 2010, vol. B 346, pp. 1581–1592.Google Scholar
  43. Lloyd, S., Carrick, F., and Hall, L., Ultrastructure of the Mature Spermatozoon of the Musky Rat-Kangaroo, Hypsiprymnodon (Potoroidae: Marsupilia), Acta Zoologica (Stockholm), 2002, vol., 83, pp. 167–174.CrossRefGoogle Scholar
  44. Meikar, O., Da Ros, M., Liljenbäck, H., Toppari, J., and Kotaja, N., Accumulation of piRNAs in the Chromatoid Bodies Purified by a Novel Isolation Protocol, Exp. Cell Res., 2010, vol. 316, pp. 1567–1575.PubMedCrossRefGoogle Scholar
  45. Meistrich, M.L., Nuclear Morphogenesis during Spermiogenesis, in Molecular Biology of the Male Reproductive System, New York: Acad. Press, 1993, pp. 67–97.Google Scholar
  46. Meng, W., Mushika, Y., Ichi, T., and Takeichi, M., Anchorage of Microtubule Minus Ends to Adherens Junctions Regulates Epithelial Cell-Cell Contacts, Cell, 2008, vol. 135, pp. 948–959.PubMedCrossRefGoogle Scholar
  47. Mironov, A.A., Komissarchik, Ya.Yu., and Mironov, V.A., Metody elektronnoi mikroskopii v biologii i meditsine (Electron Microscopy Methods in Biology and Medicine), St. Petersburg: Nauka, 1994.Google Scholar
  48. Mochida, K., Tres, L.L., and Kierszenbaum, A.L., Isolation of the Rat Spermatid Manchette and Its Perinuclear Ring, Devel. Biol., 1998, vol. 200, pp. 46–56.CrossRefGoogle Scholar
  49. Moreno, R.D., Palomino, J., and Schatten, G., Assembly of Spermatid Acrosome Depends on Microtubule Organization during Mammalian Spermiogenesis, Dev. Biol., 2006, vol. 293, pp. 218–227.PubMedCrossRefGoogle Scholar
  50. Mosevitsky, M.I. and Silicheva, I.A., Subcellular and Regional Location of “Brain” Proteins BASP1 and MARCKS in Kidney and Testis, Acta Histochem., 2011, vol. 113, pp. 13–18.PubMedCrossRefGoogle Scholar
  51. Mosevitsky, M.I., Capony, J.P., Skladchikova, G.Y., Novitskaya, V.A., Plekhanov, A.Y., and Zakharov, V.V., The BASP1 Family of Myristoylated Proteins Abundant in Axonal Termini. Primary Structure Analysis and Physico-Chemical Properties, Biochimie, 1997, vol. 79, pp. 373–384.PubMedCrossRefGoogle Scholar
  52. Mosevitsky, M.I., Nerve Ending “Signal” Proteins GAP-43, MARCKS, and BASP1, Int. Rev. Cytol., 2005, vol. 245, pp. 245–325.PubMedCrossRefGoogle Scholar
  53. Mosevitsky, M.I., Novitskaya, V.A., Plekhanov, A.Yu., and Skladchikova, G.Yu., Neuronal Protein GAP-43 Is a Member of Novel Group of Brain Acid-Soluble Proteins (BASPs), Neurosci. Res., 1994, vol. 19, pp. 223–228.PubMedCrossRefGoogle Scholar
  54. Mosevitsky, M.I., Snigirevskaya, E.S., and Komissarchik, Ya.Yu., Immune Electron Microscopic Study of Location of Proteins BASP1 and MARCKS in the Early and Late Rat Spermatids, Acta Histochem., 2011, Epub. July 15.Google Scholar
  55. Nakagawa, Y., Yamane, Y., Okanoue, T., and Tsikuta, S., Outer Dense Fiber 2 is a Widespread Centrosome Scaffold Component Preferentially Associated with Mother Centrioles: Its Identification from Isolated Centrosomes, Mol. Biol. Cell, 2001, vol. 12, pp. 1687–1697.PubMedGoogle Scholar
  56. Noce, T., Okamoto-Ito, S., and Tsuekawa, N., VASA Homolog Genes in Mammalian Germ Cell Development, Cell Struct. Funct., 2001, vol. 26, pp. 131–136.PubMedCrossRefGoogle Scholar
  57. Novitskaya, V.A., Skladchikova, G.Iu., Plekhanov, A.Iu., and Mosevitskii, M.I., Detection of BASP1 Brain Protein in Rat Reproductive Tissue, Dokl. Akad. Nauk, 1994, vol. 335, pp. 101–102.Google Scholar
  58. Paniagua, R., Nistal, M., Amat, P., and Rodriguez, M.C., Presence of Ribonucleoproteins and Basic Proteins in the Nuage and Intermitochondrial Bars of Human Spermatogonia, J. Anat., 1985, vol. 143, pp. 201–206.PubMedGoogle Scholar
  59. Parvinen, M. and Jokelainen, P.T., Rapid Movements of the Chromatoid Body in Living Early Spermatids of the Rat, Biol. Reprod., 1974, vol. 11, pp. 85–92.PubMedCrossRefGoogle Scholar
  60. Parvinen, M., Salo, J., Tivonen, M., Nevalainen, O., Soini, E., and Pelliniemi, L.J., Computer Analysis of Living Cells: Movements of the Chromatoid Body in Early Spermatids Compares with Its Ultrastructure in Snap-Frozen Preparations, Histochem. Cell Biol., 1997, vol. 108, pp. 77–81.PubMedCrossRefGoogle Scholar
  61. Parvinen, M., The Chromatoid Body in Spermatogenesis, Int. J. Androl., 2005, vol. 28, pp. 189–201.PubMedCrossRefGoogle Scholar
  62. Peruquetti, R.L., Assis, I.M., Taboga, S.R., and de Azeredo-Oliveira, M.T.V., Meiotic Nucleolar Cycle and Chromatoid Body Formation During the Rat (Rattus novergicus) and Mouse (Mus musculus) Spermiogenesis, Micron, 2009, vol. 39, pp. 419–425.CrossRefGoogle Scholar
  63. Petersen, C., Fuzesi, L., and Hoyer-Fender, S., Outer Dense Fibre Proteins from Human Sperm Tail: Molecular Cloning and Expression Analyses of Two cDNA Transcripts Encoding Proteins of ∼70 kDa, Mol. Human. Reprod., 1999, vol. 5, pp. 627–635.CrossRefGoogle Scholar
  64. Redenbach, D.M., Boekelheide, K., and Vogl, A.W., Binding between Mammalian Spermatid-Ectoplasmic Specialization Complexes and Microtubules, Eur. J. Cell Biol., 1992, vol. 59, pp. 433–448.PubMedGoogle Scholar
  65. Ricci, M., Breed, W.G., Isolation and Partial Characterization of the Outer Dense Fibres and Fibrous Sheath from the Sperm Tail of a Marsupial: The Brushtail Possum (Trichosurus vulpecula), Reproduction, 2001, vol. 121, pp. 373–388.PubMedCrossRefGoogle Scholar
  66. Rios, R.M., Sanchis, A., Tasin, A.M., Feedriani, C., and Bornens, M., GMAP-210 Recruits gamma-Tubulin Complexes to Cis-Golgi Membranes and Is Required for Golgi Ribbon Formation, Cell, 2004, vol. 118, pp. 323–335.PubMedCrossRefGoogle Scholar
  67. Rouelle-Rossier, V.B., Biggiogera, M., and Fakan, S.J., Ultrastructural Detection of Calcium and Magnesium in the Chromatoid Body of Mouse Spermatids by Electron Spectroscopic Imaging and Electron Energy Loss Spectroscopy, Histochem. Cytochem., 1993, vol. 41, pp. 1155–1162.CrossRefGoogle Scholar
  68. Russell, L. and Frank, B., Ultrastructural Characterization of Nuage in Spermatocytes of the Rat Testis, Anat. Rec., 1978, vol. 190, pp. 79–97.PubMedCrossRefGoogle Scholar
  69. Söderström, K.O., The Relationship Between the Nuage and the Chromatoid Body during Spermatogenesis in the Rat, Cell Tissue Res, 1981, vol. 15, pp. 425–430.Google Scholar
  70. Sanchez-Niño, M.D., Sanz, A.B., Lorz, C., Gnirke, A., Rastaldi, M.P., Nair, V., Egido, J., Ruiz-Ortega, M., Kretzler, M, and Ortiz, A., BASP1 Promotes Apoptosis in Diabetic Nephropathy, J. Am. Soc. Nephrol., 2010, vol. 21, pp. 610–621.PubMedCrossRefGoogle Scholar
  71. Shao, X., Tarnasky, H.A., Lee, J.P., Oko, R., and van der Hoorn, F.A., Spag4, a Novel Sperm Protein, Binds Outer Dense-Fiber Protein Odf1 and Localizes to Microtubules of Manchette and Axoneme, Dev. Biol., 1999, vol. 211, pp. 109–123.PubMedCrossRefGoogle Scholar
  72. Shao, X., Tarnasky, H.A., Schalles, U., Oko, R., and van der Hoorn, F.A., Interactions Cloning of the 84-kDa Major Outer Dense Fiber Protein Odf84, J. Biol. Chem., 1997, vol. 272, pp. 6105–6113.PubMedCrossRefGoogle Scholar
  73. Shibata, N., Tsunekawa, N., Okamoto-Ito, S., Akasu, R., Tokumaso, A., and Noce, T., Mouse RanBPM Is a Partner Gene to a Germline Specific RNA Helicase, Mouse VASA Homolog Protein, Mol. Reproduct. Develop., 2004, vol. 67, pp. 1–7.CrossRefGoogle Scholar
  74. Snigirevskaya, E.S. and Komissarchik, Ya.Yu., Noncentrosomal Microtubules in Epitheliocytes under Change in Water Permeability, Biol. Mebrany, 2003, vol. 20, pp. 41–45.Google Scholar
  75. Swan, M.A. and Alboghobeish, N., Improved Preservation of the Ram Spermatozoan Plasma Membrane Using Betaine in the Primary Fixative, J. Microsc., 1997, vol. 187, pp. 167–169.PubMedCrossRefGoogle Scholar
  76. Tarnasky, H., Cheng, M., Ou, Y., Thundathil, J.C., Oko, R., and van der Hoorn, F.A., Gene Trap Mutation of Murine Outer Dense Fiber Protein-2 Gene Can Result in Sperm Tail Abnormalities in Mice with High Percentage Chimaerism, B.M.C. Dev. Biol., 2010, vol. 10, p. 67.Google Scholar
  77. Thorne-Tjomsland, G., Clermont, Y., and Hermo, L., Contribution of the Golgi Apparatus Components to the Formation of the Acrosomic System and Chromatoid Body in Rat Spermatids, Anat. Rec., 1988, vol. 222, pp. 590–598.Google Scholar
  78. Tres, L.L., Kierzsenbaum, A.L., Sak57, an Acidic Keratin Initially Present in the Spermatid Manchette before Becoming a Component of Paraaxonemal Structures of the Developing Tail, Mol. Reprod. Dev., 1996, vol. 44, pp. 395–407.PubMedCrossRefGoogle Scholar
  79. Vasileva, A., Tiedau, D., Firooznia, A., Müller-Reichert, T., and Jessberger, R., Tdrd6 Is Required for Spermiogenesis, Chromatoid Body Architecture, and Regulation of miRNA Expression, Curr. Biol., 2009, vol. 19, pp. 630–639.PubMedCrossRefGoogle Scholar
  80. Ventela, S., Toppari, J., and Parvinen, M., Intercellular Organelle Traffic through Cytoplasmic Bridges in Early Spermatids of the Rat: Mechanisms of Haploid Gene Product Sharing, Mol. Biol. Cell, 2003, vol. 14, pp. 2768–2780.PubMedCrossRefGoogle Scholar
  81. Vogl, A.W., Vaid, K.S., and Guttman, J., The Sertoli Cell Cytoskeleton, in Molecular Mechanisms in Spermatogenesis, Cheng, C.Y., Ed., Austin, TX: Landes Bioscience/Springer Science+Business Media LLC, 2008, pp. 186–211.Google Scholar
  82. Vogl, A.W., Pfeiffer, D.C., Mulholland, D., Kimel, G., and Guttman, J., Unique and Multifunctional Adhesion in the Testis: Ectoplasmic Specializations, Arch. Histol. Cytol., 2000, vol. 63,1, pp. 1–15.PubMedCrossRefGoogle Scholar
  83. Wang, F., Zhang, Q., Cao, J., Huang, Q., and Zhu, X., The Microtubule Plus End-Binding Protein EB1 Is Involved in Sertoli Cell Plasticity in Testicular Seminiferous Exptl, Cell Res.,, 2008, vol. 314, pp. 213–226.CrossRefGoogle Scholar
  84. Xiao, X. and Yang, W., Actin-Based Dynamics during Spermatogenesis and Its Significance, J. Zhejiang Univ. Sci., 2007, vol. B8, pp. 498–506.Google Scholar
  85. Xu, B., Hao, Z., Jha, K.N., Zhang, Z., Urekar, Z., Digilio, L., Pulido, S., Strauss J.F., III, Flickinger, C., and Herr, J.C., TSKS Concentrates in Spermatid Centrioles during Flagellogenesis, Develop. Biol., 2008, vol. 319, pp. 201–210.PubMedCrossRefGoogle Scholar
  86. Yao, R., Ito, C., Natsume, Y., Sugitni, Y., Yamanaka, H., Kuretake, S., Yangida, K., Sato, A., and Toshimori Knoda, T., Lack of Acrosome Formation in Mice Lacking Golgi Protein, GOPC, Proc. Natl. Acad. Sci. USA, 2002, vol. 99, pp. 11211–11216.PubMedCrossRefGoogle Scholar
  87. Zakharov, V.V., Capony, J.P., Derancourt, J., Kropolova, E.S., Novitskaya, V.A., Bogdanova, M.N., and Mosevitsky, M.I., Natural N-Terminal Fragments of Brain Abundant Myristoylated Protein BASP1, Biochim. Biophys. Acta, 2003, vol. 1622, pp. 14–19.PubMedCrossRefGoogle Scholar
  88. Zakharov, V.V., Mosevitsky, M.I., Oligomeric Structure of Brain Abundant Proteins GAP-43 and BASP1, J. Struct. Biol., 2010, vol. 170, pp. 470–483.PubMedCrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2012

Authors and Affiliations

  • E. S. Snigirevskaya
    • 1
  • M. I. Mosevitsky
    • 2
  • Ya. Yu. Komissarchik
    • 1
  1. 1.Institute of Cytology, Russian Academy of SciencesSt. PetersburgRussia
  2. 2.St. Petersburg Institute of Nuclear PhysicsRussian Academy of SciencesSt. PetersburgRussia

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