Skip to main content
Log in

Role of microtubule-dependent membrane trafficking in acrosomal biogenesis

  • Regular Article
  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Abstract

The role of microtubule-based trafficking in acrosomal biogenesis was examined by studying the effects of colchicine on spermiogenesis. In electron micrographs of untreated cap-phase mouse spermatids, coated vesicles were always seen on the apex and caudal margins of the developing acrosomal cap. The increase in volume and the accumulation of materials in the acrosome during the Golgi and cap phases were observed to occur via fusion of vesicles at various sites on the growing acrosome. By studying the acid phosphatase localization pattern and colchicine-treated spermatids, the role of clathrin-coated vesicles became clear. Coated vesicle formation at the caudal margin of the acrosome appeared to be responsible for the spreading and shaping of the acrosome over the surface of the nucleus and also established distinct regional differences in the acrosome. In colchicine-treated spermatids, the Golgi apparatus lost its typical membranous stack conformation and disintegrated into many small vesicles. Acrosome formation was retarded, and there was discordance of the spread of the acrosomal cap with that of the modified nuclear envelope. Many symplasts were also found because of the breakdown of intercellular bridges. Colchicine treatment thus indicated that microtubule-dependent trafficking of transport vesicles between the Golgi apparatus and the acrosome plays a vital role in acrosomal biogenesis. In addition, both anterograde and retrograde vesicle trafficking are extensively involved and seem to be equally important in acrosome formation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Bonifacino JS, Glick BS (2004) The mechanisms of vesicle budding and fusion. Cell 116:153–166

    Article  PubMed  CAS  Google Scholar 

  • Bozzola JJ, Polakoski K, Haas N, Russell LD, Campbell P, Peterson RN (1991) Localization of boar sperm proacrosin during spermatogenesis and during sperm maturation in the epididymis. Am J Anat 192:129–141

    Article  PubMed  CAS  Google Scholar 

  • Clermont Y, Leblond CP (1955) Spermiogenesis of man, monkey, ram and other mammals as shown by the periodic acid-Schiff technique. Am J Anat 96:229–253

    Article  PubMed  CAS  Google Scholar 

  • Dell KR (2003) Dynactin polices two-way organelle traffic. J Cell Biol 160:291–293

    Article  PubMed  CAS  Google Scholar 

  • Fouquet JP, Valentin A, Kann ML (1992) Perinuclear cytoskeleton of acrosome-less spermatids in the blind sterile mutant mouse. Tissue Cell 24:655–665

    Article  PubMed  CAS  Google Scholar 

  • Friend DS, Fawcett DW (1974) Membrane differentiations in freeze-fractured mammalian sperm. J Cell Biol 63:641–664

    Article  PubMed  CAS  Google Scholar 

  • Galli T, Haucke V (2004) Cycling of synaptic vesicles: how far? How fast! Sci STKE 264:1–12

    Google Scholar 

  • Griffiths G, Warren G, Stuhlfauth I, Jockusch BM (1981) The role of clathrin-coated vesicles in acrosome formation. Eur J Cell Biol 26:52–60

    PubMed  CAS  Google Scholar 

  • Griffiths GW (1979) Transport of glial cell acid phosphatase by endoplasmic reticulum into damaged axons. J Cell Sci 36:361–389

    PubMed  CAS  Google Scholar 

  • Handel MA (1979) Effects of colchicine on spermiogenesis in the mouse. J Embryol Exp Morphol 51:73–83

    PubMed  CAS  Google Scholar 

  • Ho HC, Tang CY, Suarez SS (1999) Three-dimensional structure of the Golgi apparatus in mouse spermatids: a scanning electron microscopic study. Anat Rec 256:189–194

    Article  PubMed  CAS  Google Scholar 

  • Holt WV (1979) Development and maturation of the mammalian acrosome. A cytochemical study using phosphotungstic acid staining. J Ultrastruct Res 68:58–71

    Article  PubMed  CAS  Google Scholar 

  • Jordens I, Fernandez-Borja M, Marsman M, Dusseljee S, Janssen L, Calafat J, Janssen H, Wubbolts R, Neefjes J (2001) The Rab7 effector protein RILP controls lysosomal transport by inducing the recruitment of dynein-dynactin motors. Curr Biol 11:1680–1685

    Article  PubMed  CAS  Google Scholar 

  • Kierszenbaum AL, Rivkin E, Tres LL (2003) Acroplaxome, an F—actin—keratin—containing plate, anchors the acrosome to the nucleus during shaping of the spermatid head. Mol Biol Cell 14:4628–4640

    Article  PubMed  CAS  Google Scholar 

  • Kierszenbaum AL, Tres LL (2004) The acrosome—acroplaxome—manchette complex and the shaping of the spermatid head. Arch Histol Cytol 67:271–284

    Article  PubMed  CAS  Google Scholar 

  • Kraemer J, Schmitz F, Drenckhahn D (1999) Cytoplasmic dynein and dynactin as likely candidates for microtubule-dependent apical targeting of pancreatic zymogen granules. Eur J Cell Biol 78:265–277

    PubMed  CAS  Google Scholar 

  • Leblond CP, Clermont Y (1952) Spermiogenesis of rat, mouse, hamster and guinea pig as revealed by the “periodic acid-fuchsin sulfurous acid” technique. Am J Anat 90:167–215

    Article  PubMed  CAS  Google Scholar 

  • Moreno RD, Ramalho-Santos J, Sutovsky P, Chan EK, Schatten G (2000) Vesicular traffic and Golgi apparatus dynamics during mammalian spermatogenesis: implications for acrosome architecture. Biol Reprod 63:89–98

    Article  PubMed  CAS  Google Scholar 

  • Moreno RD, Schatten G (2000) Microtubule configurations and post-translational alpha-tubulin modifications during mammalian spermatogenesis. Cell Motil Cytoskeleton 46:235–246

    Article  PubMed  CAS  Google Scholar 

  • Parvinen M, Wright WW, Phillips DM, Mather JP, Musto NA, Bardin CW (1983) Spermatogenesis in vitro: completion of meiosis and early spermiogenesis. Endocrinology 112:1150–1152

    Article  PubMed  CAS  Google Scholar 

  • Pelletier RM, Friend DS (1983) Development of membrane differentiations in the guinea pig spermatid during spermiogenesis. Am J Anat 167:119–141

    Article  PubMed  CAS  Google Scholar 

  • Peterson RN, Bozzola J, Polakoski K (1992) Protein transport and organization of the developing mammalian sperm acrosome. Tissue Cell 24:1–15

    Article  PubMed  CAS  Google Scholar 

  • Ramalho-Santos J, Moreno RD, Wessel GM, Chan EK, Schatten G (2001) Membrane trafficking machinery components associated with the mammalian acrosome during spermiogenesis. Exp Cell Res 267:45–60

    Article  PubMed  CAS  Google Scholar 

  • Rindler MJ, Ivanov IE, Sabatini DD (1987) Microtubule-acting drugs lead to the nonpolarized delivery of the influenza hemagglutinin to the cell surface of polarized Madin-Darby canine kidney cells. J Cell Biol 104:231–241

    Article  PubMed  CAS  Google Scholar 

  • Russell LD, Lee IP, Ettlin R, Peterson RN (1983) Development of the acrosome and alignment, elongation and entrenchment of spermatids in procarbazine-treated rats. Tissue Cell 15:615–626

    Article  PubMed  CAS  Google Scholar 

  • Russell LD, Malone JP, MacCurdy DS (1981) Effect of the microtubule disrupting agents, colchicine and vinblastine, on seminiferous tubule structure in the rat. Tissue Cell 13:349–367

    Article  PubMed  CAS  Google Scholar 

  • Russell LD, Russell JA, MacGregor GR, Meistrich ML (1991) Linkage of manchette microtubules to the nuclear envelope and observations of the role of the manchette in nuclear shaping during spermiogenesis in rodents. Am J Anat 192:97–120

    Article  PubMed  CAS  Google Scholar 

  • Russell LD, Ying L, Overbeek PA,(1994) Insertional mutation that causes acrosomal hypo-development: its relationship to sperm head shaping. Anat Rec 238:437–453

    Article  PubMed  CAS  Google Scholar 

  • Schnapp BJ, Vale RD, Sheetz MP, Reese TS (1985) Single microtubules from squid axoplasm support bidirectional movement of organelles. Cell 40:455–462

    Article  PubMed  CAS  Google Scholar 

  • Sheetz MP, Vale R, Schnapp B, Schroer T, Reese T (1987) Movements of vesicles on microtubules. Ann N Y Acad Sci 493:409–416

    Article  PubMed  CAS  Google Scholar 

  • Sinowatz F, Wrobel KH (1981) Development of the bovine acrosome. An ultrastructural and cytochemical study. Cell Tissue Res 219:511–524

    Article  PubMed  CAS  Google Scholar 

  • Sotomayor RE, Handel MA (1986) Failure of acrosome assembly in a male sterile mouse mutant. Biol Reprod 34:171–182

    Article  PubMed  CAS  Google Scholar 

  • Stackpole CW, Devorkin D (1974) Membrane organization in mouse spermatozoa revealed by freeze-etching. J Ultrastruct Res 49:167–187

    Article  PubMed  CAS  Google Scholar 

  • Tanaka K (1989) High resolution scanning electron microscopy of the cell. Biol Cell 65:89–98

    Article  PubMed  CAS  Google Scholar 

  • Tang XM, Lalli MF, Clermont Y (1982) A cytochemical study of the Golgi apparatus of the spermatid during spermiogenesis in the rat. Am J Anat 163:283–294

    Article  PubMed  CAS  Google Scholar 

  • Tanii I, Yoshinaga K, Toshimori K (1998) The effects of brefeldin A on acrosome formation and protein transport to the acrosome in organ cultures of rat seminiferous tubules. J Electron Microsc 47:161–167

    CAS  Google Scholar 

  • Thyberg J, Moskalewski S (1985) Microtubules and the organization of the Golgi complex. Exp Cell Res 159:1–16

    Article  PubMed  CAS  Google Scholar 

  • Ventela S, Mulari M, Okabe M, Tanaka H, Nishimune Y, Toppari J, Parvinen M (2000) Regulation of acrosome formation in mice expressing green fluorescent protein as a marker. Tissue Cell 32:501–507

    Article  PubMed  CAS  Google Scholar 

  • Weber JE, Russell LD (1987) A study of intercellular bridges during spermatogenesis in the rat. Am J Anat 180:1–24

    Article  PubMed  CAS  Google Scholar 

  • Yamaguchi N, Takanezawa Y, Koizumi H, Umezu-Goto M, Aoki J, Arai H, (2004) Expression of NUDEL in manchette and its implication in spermatogenesis. FEBS Lett 566:71–76

    Article  PubMed  CAS  Google Scholar 

  • Yanagimachi R (1994) Mammalian fertilization. In: Knobil E, Neill J (eds) The physiology of reproduction. Raven, New York, pp 189–317

    Google Scholar 

  • Yang WX, Sperry AO (2003) C-terminal kinesin motor KIFC1 participates in acrosome biogenesis and vesicle transport. Biol Reprod 69:1719–1729

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We express our gratitude to our mentors Jia-Chyuan Chen and Hsiao-Hsu Jen for introducing us to the world of electron microscopy. We also thank Dr. Susan S. Suarez for critical review of the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Han-Chen Ho.

Additional information

This work was supported by grants 83-0211-B-002-184 and 93-2320-B-320-012 from the National Science Council, Taiwan, Republic of China.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Huang, WP., Ho, HC. Role of microtubule-dependent membrane trafficking in acrosomal biogenesis. Cell Tissue Res 323, 495–503 (2006). https://doi.org/10.1007/s00441-005-0097-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00441-005-0097-9

Keywords

Navigation