Brain synaptic junctional proteins at the acrosome of rat testicular germ cells

Journal of Histochemistry and Cytochemistry

Volumn 51, Issue 6, 2003, Pages 809-819

  Redecker, Peter ^a   Kreutz, Michael R ^b   Bockmann, Jürgen ^c   Gundelfinger, Eckart D ^b   Boeckers, Tobias M ^b,c  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b LEIBNIZ INSTITUTE FOR NEUROBIOLOGY   (Germany)

^c UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

Acrosome; Chemical synapse; Complexin; GABA; GAD; Glutamate; Postsynaptic density; Shank; SV2; Vesicular neurotransmitter, transporters

Indexed keywords

4 AMINOBUTYRIC ACID; AMINO ACID TRANSPORTER; BRAIN PROTEIN; BRAIN SYNAPTIC JUNCTIONAL PROTEIN; COMPLEXIN; GLUTAMATE TRANSPORTER; MEMBRANE PROTEIN; PROTEIN GLAST; PROTEIN GLT1; PROTEIN SV2; UNCLASSIFIED DRUG; VESICULAR AMINO ACID TRANSPORTER;

ACROSOME; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; GERM CELL; IMMUNOGOLD ELECTRON MICROSCOPY; MALE; NONHUMAN; POSTSYNAPTIC MEMBRANE; PRESYNAPTIC NERVE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; RAT; SYNAPSE; TESTIS;

ANIMALIA;

EID: 0038100158     PISSN: 00221554     EISSN: None     Source Type: Journal    
DOI: 10.1177/002215540305100612     Document Type: Article

References (61)

1. Aanesen A, Fried G, Andersson E, Gottlieb C (1996) Carrier-mediated gamma-aminobutyric acid uptake in human spermatozoa indicating the presence of a high-affinity gamma-aminobutyric acid transport protein. Biol Reprod 54:841-846
2. Archer DA, Graham ME, Burgoyne RD (2002) Complexin regulates the closure of the fusion pore during regulated vesicle exocytosis. J Biol Chem 277:18249-18252
3. Aumüller G, Seitz J (1988) Immunocytochemical localization of actin and tubulin in rat testis and spermatozoa. Histochemistry 89:261-267
4. Bellocchio EE, Reimer RJ, Fremeau RT Jr, Edwards RH (2000) Uptake of glutamate into synaptic vesicles by an inorganic phosphate transporter. Science 289:957-960
5. Boeckers TM, Bockmann J, Kreutz MR, Gundelfinger ED (2002) ProSAP/Shank proteins - a family of higher order organizing molecules of the postsynaptic density with an emerging role in human neurological disease. J Neurochem 81:903-910
6. Boeckers TM, Kreutz MR, Winter C, Zuschratter W, Smalla K-H, Sanmarti-Vila L, Wex H, et al. (1999) Proline-rich synapse-associated protein-1/cortactin binding protein 1 (ProSAP1/CortBP1) is a PDZ-domain protein highly enriched in the postsynaptic density. J Neurosci 19:6506-6518
7. Boeckers TM, Mameza MG, Kreutz MR, Bockmann J, Weise C, Buck F, Richter D, et al. (2001) Synaptic scaffolding proteins in rat brain. Ankyrin repeats of the multidomain shank protein family interact with the cytoskeletal protein α-fodrin. J Biol Chem 276:40104-40112
8. - channel in the acrosome reaction initiated by recombinant ZP3. Biol Reprod 66:91-97
9. Chaudhry FA, Reimer RJ, Bellocchio EE, Danbolt NC, Osen KK, Edwards RH, Storm-Mathisen J (1998) The vesicular GABA transporter, VGAT, localizes to synaptic vesicles in sets of glycinergic as well as GABAergic neurons. J Neurosci 18:9733-9750
10. Du Y, Weed SA, Wen-Cheng X, Marshall TD, Parsons TJ (1998) Identification of a novel cortactin SH3 domain-binding protein and its localization to growth cones of cultured neurons. Mol Cell Biol 18:5838-5851
11. Dumoulin A, Rostaing P, Bedet C, Lévi S, Isambert M-F, Henry J-P, Triller A, et al. (1999) Presence of the vesicular inhibitory amino acid transporter in GABAergic and glycinergic synaptic terminal boutons. J Cell Sci 112:811-823
12. Feldblum S, Dumoulin A, Anoal M, Sandillon F, Privat A (1995) Comparative distribution of GAD65 and GAD67 mRNAs and proteins in the rat spinal cord supports a differential regulation of these two glutamate decarboxylases in vivo. J Neurosci Res 42:742-757
13. Fremeau RT Jr, Troyer MD, Pahner I, Nygaard GO, Tran CH, Reimer RJ, Bellocchio EE, et al. (2001) The expression of vesicular glutamate transporters defines two classes of excitatory synapse. Neuron 31:247-260
14. Fujiyama F, Furuta T, Kaneko T (2001) Immunocytochemical localization of candidates for vesicular glutamate transporters in the rat cerebral cortex. J Comp Neurol 435:379-387
15. Herzog E, Bellenchi GC, Gras C, Bernard V, Ravassard P, Bedet C, Gasnier B, et al. (2001) The existence of a second vesicular glutamate transporter specifies subpopulations of glutamatergic neurons. J Neurosci 21:181-186
16. Hinton BT (1990) The testicular and epididymal luminal amino acid microenvironment in the rat. J Androl 11:498-505
17. Hu JH, He XB, Wu Q, Yan YC, Koide SS (2002) Subunit composition and function of GABA receptors of rat spermatozoa. Neurochem Res 27:195-199
18. Hu JH, He XB, Yan YC (2000) Identification of gamma-aminobutyric acid transporter (GAT1) on the rat sperm. Cell Res 10:51-58
19. Hua MY, Hu JH, Zhou XG, Mei ZT, Fei J, Guo LH (2000) γ-Aminobutyric acid transporter (GAT1) overexpression in mouse affects the testicular morphology. Cell Res 10:59-69
20. Hutt DM, Cardullo RA, Baltz JM, Ngsee JK (2002) Synaptotagmin VIII is localized to the mouse sperm head and may function in acrosomal exocytosis. Biol Reprod 66:50-56
21. Jakobsen A-M, Ahlman H, Wängberg B, Kölby L, Bengtsson M, Nilsson O (2002) Expression of synaptic vesicle protein 2 (SV2) in neuroendocrine tumours of the gastrointestinal tract and pancreas. J Pathol 196:44-50
22. Kierszenbaum AL (2000) Fusion of membranes during the acrosome reaction: a tale of two SNAREs. Mol Reprod Dev 57:309-310
23. 2+-binding protein caldendrin: gene structure, splice isoforms, and expression in the rat central nervous system. Mol Cell Neurosci 19:459-475
24. Lehre KP, Levy LM, Ottersen OP, Storm-Mathisen J, Danbolt NC (1995) Differential expression of two glial glutamate transporters in the rat brain. Quantitative and immunocytochemical observations. J Neurosci 15:1835-1853
25. Lim S, Naisbitt S, Yoon J, Hwang J-I, Suh P-G, Sheng M, Kim E (1999) Characterization of the Shank family of synaptic proteins. J Biol Chem 274:29510-29518
26. Liu DY, Martic M, Clarke GN, Grkovic I, Garrett C, Dunlop ME, Baker HWG (2002) An anti-actin monoclonal antibody inhibits the zona pellucida-induced acrosome reaction and hyperactivated motility of human sperm. Mol Hum Reprod 8:37-47
27. Martínez-Menárguez JA, Geuze HJ, Ballesta J (1996) Evidence for a nonlysosomal origin of the acrosome. J Histochem Cytochem 44:313-320
28. Meizel S (1997) Amino acid neurotransmitter receptor/chloride channels of mammalian sperm and the acrosome reaction. Biol Reprod 56:569-574
29. - channel in porcine sperm. Biochem Biophys Res Commun 223:675-678
30. Michaut M, De Blas G, Tomes CN, Yunes R, Fukuda M, Mayorga LS (2001) Synaptotagmin VI participates in the acrosome reaction of human spermatozoa. Dev Biol 235:521-529
31. Naisbitt S, Kim E, Tu JC, Xiao B, Sala C, Valtschanoff J, Weinberg RJ, et al. (1999) Shank, a novel family of postsynaptic density proteins that binds to the NMDA receptor/PSD-95/GKAP complex and cortactin. Neuron 23:569-582
32. Pabst S, Margittai M, Vainius D, Langen R, Jahn R, Fasshauer D (2002) Rapid and selective binding to the synaptic SNARE complex suggests a modulatory role of complexins in neuroexocytosis. J Biol Chem 277:7838-7848
33. Pabst H, Redecker P (1999) Interstitial glial cells of the gerbil pineal gland display immunoreactivity for the metabotropic glutamate receptors mGluR2/3 and mGluR5. Brain Res 838:60-68
34. Paranko J, Yagi A, Kuusisto M (1994) Immunocytochemical detection of actin and 53 kDa polypeptide in the epididymal spermatozoa of rat and mouse. Anat Rec 240:516-527
35. Persson H, Pelto-Huikko M, Metsis M, Söder O, Brené S, Skog S, Hökfelt T, et al. (1990) Expression of the neurotransmitter-synthesizing enzyme glutamic acid decarboxylase in male germ cells. Mol Cell Biol 10:4701-4711
36. Ramalho-Santos J, Moreno RD, Wessel GM, Chan EKL, Schatten G (2001) Membrane trafficking machinery components associated with the mammalian acrosome during spermiogenesis. Exp Cell Res 267:45-60
37. Redecker P (1993) Dense accumulations of synaptic-like microvesicles in "dark" pinealocytes of the gerbil pineal gland. J Neurocytol 22:572-581
38. Redecker P (1996) Synaptotagmin I, synaptobrevin II, and syntaxin I are coexpressed in rat and gerbil pinealocytes. Cell Tissue Res 283:443-454
39. Redecker P (1999) Immunoreactivity for multiple GABA transporters (GAT-1, GAT-2, GAT-3) in the gerbil pineal gland. Neurosci Lett 266:117-120
40. Redecker P, Bargsten G (1993) Synaptophysin - A common constituent of presumptive secretory microvesicles in the mammalian pinealocyte: a study of rat and gerbil pineal glands. J Neurosci Res 34:79-96
41. Redecker P, Pabst H (2000) Immunohistochemical study of the glutamate transporter proteins GLT-1 and GLAST in rat and gerbil pineal gland. J Pineal Res 28:179-184
42. Redecker P, Cetin Y, Korf H-W (1996) Differential immunocytochemical localization of calretinin in the pineal gland of three mammalian species. J Neurocytol 25:9-18
43. Redecker P, Gundelfinger ED, Boeckers TM (2001a) The cortactin-binding postsynaptic density protein ProSAP1 in non-neuronal cells. J Histochem Cytochem 49:639-648
44. Redecker P, Pabst H, Löscher W, Steinlechner S (2001b) Evidence for microvesicular storage and release of glycine in rodent pinealocytes. Neurosci Lett 299:93-96
45. Rothstein JD, Dykes-Hoberg M, Pardo CA, Bristol LA, Jin L, Kuncl RW, Kanai Y, et al. (1996) Knockout of glutamate transporters reveals a major role for astroglial transport in excitotoxicity and clearance of glutamate. Neuron 16:675-686
46. Rothstein JD, Martin L, Levey AI, Dykes-Hoberg M, Jin L, Wu D, Nash N, et al. (1994) Localization of neuronal and glial glutamate transporters. Neuron 13:713-725
47. Sato Y, Son JH, Meizel S (2000) The mouse sperm glycine receptor/chloride channel: cellular localization and involvement in the acrosome reaction initiated by glycine. J Androl 21:99-106
48. Seidenbecher CI, Langnaese K, Sanmarti-Vila L, Boeckers TM, Smalla K-H, Sabel BA, Garner CC, et al. (1998) Caldendrin, a novel neuronal calcium-binding protein confined to the somatodendritic compartment. J Biol Chem 273:21324-21331
49. Sheng M, Kim E (2000) The Shank family of scaffold proteins. J Cell Sci 113:1851-1856
50. Storto M, Sallese M, Salvatore L, Poulet R, Condorelli DF, Dell'Albani P, Marcello MF, et al. (2001) Expression of metabotropic glutamate receptors in the rat and human testis. J Endocrinol 170:71-78
51. Sun-Wada G-H, Imai-Senga Y, Yamamoto A, Murata Y, Hirata T, Wada Y, Futai M (2002) A proton pump ATPase with testis-specific E1 subunit isoform required for acrosome acidification. J Biol Chem 277:18098-18105
52. Syntin P, Cornwall GA (1999) Immunolocalization of CRES (cystatin-related epididymal spermatogenic) protein in the acrosomes of mouse spermatozoa. Biol Reprod 60:1542-1552
53. Takamori S, Rhee JS, Rosenmund C, Jahn R (2000) Identification of a vesicular glutamate transporter that defines a glutamatergic phenotype in neurons. Nature 407:189-194
54. Takamori S, Rhee JS, Rosenmund C, Jahn R (2001) Identification of differentiation-associated brain-specific phosphate transporter as a second vesicular glutamate transporter (VGLUT2). J Neurosci 21:182-187
55. 67. J Neurochem 58:618-627
56. Tomes CN, Michaut M, De Blas G, Visconti P, Matti U, Mayorga LS (2002) SNARE complex assembly is required for human sperm acrosome reaction. Dev Biol 243:326-338
57. Tu JC, Xiao B, Naisbitt S, Yuan JP, Petralia RS, Brakeman P, Doan A, et al. (1999) Coupling of mGluR/Homer and PSD-95 complexes by the shank family of postsynaptic density proteins. Neuron 23:583-592
58. Ward CR, Faundes D, Foster LA (1999) The monomeric GTP binding protein, rab3a, is associated with the acrosome in mouse sperm. Mol Reprod Dev 53:413-421
59. Wassarman PM (1999) Mammalian fertilization: molecular aspects of gamete adhesion, exocytosis, and fusion. Cell 96:175-183
60. - channel complex in the progesterone-initiated acrosome reaction. Dev Biol 159:679-690
61. Xu T, Bajjalieh SM (2001) SV2 modulates the size of the readily releasable pool of secretory vesicles. Nature Cell Biol 3:691-698