The Golgi apparatus segregates from the lysosomal/acrosomal vesicle during rhesus spermiogenesis: Structural alterations

Developmental Biology

Volumn 219, Issue 2, 2000, Pages 334-349

  Moreno, Ricardo D ^a   Ramalho Santos, João ^a   Chan, Edward K L ^b   Wessel, Gary M ^c   Schatten, Gerald ^a,d  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c BROWN UNIVERSITY   (United States)

^d OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Acrosin; Acrosome biogenesis; Golgi apparatus; Spermatid

Indexed keywords

FLUORESCENT DYE; HYDROLASE; POLYCLONAL ANTIBODY;

ACROSOME; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL ORGANELLE; CONTROLLED STUDY; GOLGI COMPLEX; MALE; MONKEY; NONHUMAN; PRIORITY JOURNAL; SPERMATID; SPERMATOGENESIS; ZONA PELLUCIDA;

ANIMALIA; MACACA MULATTA; PRIMATES;

EID: 0034643141     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1006/dbio.2000.9606     Document Type: Article

References (82)

1. Barr F. A. A novel Rab6-interacting domain defines a family of Golgi-targeted coiled-coil proteins. Curr. Biol. 9:1999;381-384.
2. Barros C., Crosby J. A., Moreno R. D. Early steps of sperm-egg interactions during mammalian fertilization. Cell Biol. Int. 20:1996;33-39.
3. Bavister B. D., Boatman D. E., Leibfried L., Loose M., Vernon M. W. Fertilization and cleavage of rhesus monkey oocytes in vitro. Biol. Reprod. 28:1983;983-999.
4. Boatman D. E. In vitro growth of non-human primate pre- and peri-implantation embryos. Bavister B. D. The Mammalian Preimplantation Embryo. 1987;273-308 Plenum, New York.
5. Bowen R. H. On the idiosome, Golgi apparatus, and acrosome in the male germ cells. Anat. Rec. 24:1922;159-180.
6. Burgos M. H., Fawcett D. W. Studies on the fine structure of the mammalian testis. I. Differentiation of the spermatids in the cat (Felis domestica). J. Biophys. Biochem. Cytol. 1:1955;287-315.
7. Burgos M. H., Gutierrez L. S. The Golgi complex of the early spermatid in guinea pig. Anat. Rec. 216:1986;139-145.
8. Carnell L., Moore H. P. H. Transport via the regulated secretory pathway in semi-intact PC12 cells: Role of intra-cisternal calcium and pH in the transport and sorting of secretogranin II. J. Cell Biol. 127:1994;693-705.
9. Cole N. B., Sciaky N., Marotta A., Song J., Lippincott-Schwartz J. Golgi dispersal during microtubule disruption: Regeneration of Golgi stacks at peripheral endoplasmic reticulum exit sites. Mol. Biol. Cell. 7:1996;631-650.
10. Conner S., Leaf D., Wessel G. Members of the SNARE hypothesis are associated with cortical granule exocytosis in the sea urchin egg. Mol. Reprod. Dev. 48:1997;106-118.
11. Colomer V., Kicska G. A., Rindler M. J. Secretory granule content proteins and the luminal domains of granule membrane proteins aggregate in vitro at mildly acidic pH. J. Biol. Chem. 271:1996;48-55.
12. Cross N. L., Razy-Faulkner P. Control of human sperm intracellular pH by cholesterol and its relationship to the response of the acrosome to progesterone. Biol. Reprod. 56:1997;1169-1174.
13. de Kretser D. M. Ultrastructural features of human spermiogenesis. Z. Zellforsch. 98:1969;477-505.
14. de Kretser D. M., Kerr J. B. The cytology of the testis. Knobil E., Neill J. The Physiology of Reproduction. 1988;837-932 Raven Press, New York.
15. Dietert S. E. Fine structure of the formation and fate of the residual bodies of mouse spermatozoa with evidence for the participation of lysosomes. J. Morphol. 120:1966;317-346.
16. Demaurex N., Furuya W., D'Souza S., Bonifacino J. S., Grinstein S. Mechanism of acidification of the trans-Golgi network (TGN): In situ measurements of pH using retrieval of TGN38 and furin from the cell surface. J. Biol. Chem. 273:1998;2044-2051.
17. Escalier D., Gallo J. M., Albert M., Meduri G., Bermudez D., David G., Schrevel J. Human acrosome biogenesis: Immunodetection of proacrosin in primary spermatocytes and its partitioning pattern during meiosis. Development. 113:1991;779-788.
18. Fawcett D. W. The mammalian spermatozoon. Dev. Biol. 44:1975;394-436.
19. Fawcett D. W., Anderson W. A., Phillips D. M. Morphogenetic factors influencing the shape of the sperm head. Dev. Biol. 26:1971;220-251.
20. Fissore R. A., He C. L., Vande Woude G. F. Potential role of mitogen-activated protein kinase during meiosis resumption in bovine oocytes. Biol. Reprod. 55:1996;1261-1270.
21. Flörke S., Phi-van L., Müller-Esterl W., Scheuber H. P., Engel W. Acrosin in the spermiohistogenesis of mammals. Differentiation. 24:1983;250-256.
22. Fritzler M. J., Lung C. C., Hamel J. C., Griffith K. J., Chan E. K. L. Molecular characterization of Golgin-245, a novel Golgi complex protein containing a granin signature. J. Biol. Chem. 270:1995;31262-31268.
23. Griffith K. J., Chan E. K. L., Lung C. C., Hamel J. C., Guo X., Miyachi K., Fritzler M. J. Molecular cloning of a novel 97-kd Golgi complex autoantigen associated with Sjögrens syndrome. Arthritis Rheum. 40:1997;1693-1702.
24. Hall E. S., Eveleth J., Jiang C., Redenbach D. M., Boekelheide K. Distribution of the microtubule-dependent motors cytoplasmic dynein and kinesin in rat testis. Biol. Reprod. 46:1992;817-828.
25. Haller K., Fabry S. Brefeldin A affects synthesis and integrity of a eukaryotic flagellum. Biochem. Biophys. Res. Commun. 242:1998;597-601.
26. Haller T., Dietl P., Deetjen P., Volkl H. The lysosomal compartment as intracellular calcium store in MDCK cells: A possible involvement in InsP3-mediated Ca2+ release. Cell Calcium. 19:1996;157-165.
27. Hartree E. F. The acrosome-lysosome relationship. J. Reprod. Fertil. 44:1975;125-126.
28. Hay J. C., Chao D. S., Kuo C. S., Scheller R. H. Protein interactions regulating vesicle transport between the endoplasmic reticulum and Golgi apparatus in mammalian cells. Cell. 89:1997;149-158.
29. Hermo L., Rambourg A., Clermont Y. Three-dimensional architecture of the cortical region of the Golgi apparatus in rat spermatids. Am. J. Anat. 157:1980;357-373.
30. Hewitson L., Dominko T., Takahashi D., Martinovich C., Ramalho-Santos J., Sutovsky P., Fanton J., Jacob D., Monteith D., Neuringer M., Battaglia D., Simerly C., Schatten G. Unique checkpoints during the first cell cycle of fertilization after intracytoplasmic sperm injection in rhesus monkeys. Nature Med. 5:1999;431-433.
31. Ho W. C., Allan V. J., van Meer G., Berger E. G., Kreis T. E. Reclustering of scattered Golgi elements occurs along microtubules. Eur. J. Cell Biol. 48:1989;250-263.
32. Holstein A. F. Ultrastructural observations on the differentiation of spermatids in man. Andrologia. 8:1976;157-165.
33. Huttner W. B., Gerdes H. H., Rosa P. The granin (chromogranin/secretogranin) family. Trends Biochem. Sci. 16:1991;27-30.
34. Kashiwabara S., Arai Y., Kodaira K., Baba T. Acrosin biosynthesis in meiotic and postmeiotic spermatogenic cells. Biochem. Biophys. Res. Commun. 173:1990;240-245.
35. Keller P., Simons K. Post-Golgi biosynthetic trafficking. J. Cell Sci. 110:1997;3001-3009.
36. Kimura Y., Yanagimachi Y. Intracytoplasmic sperm injection in the mouse. Biol. Reprod. 52:1995;709-720.
37. Kjer-Nielsen L., Teasdale R. D., van Vliet C., Gleeson P. A. A novel Golgi-localisation domain shared by a class of coiled-coil peripheral membrane proteins. Curr. Biol. 9:1999;385-388.
38. Kuliawat R., Arvan P. Distinct molecular mechanisms for protein sorting within immature secretory granules of pancreatic b-cells. J. Cell Biol. 126:1994;77-86.
39. Kuliawat R., Klumperman J., Ludwig T., Arvan P. Differential sorting of lysosomal enzymes out of the regulated secretory pathway in pancreatic β-cells. J. Cell Biol. 137:1997;595-608.
40. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227:1970;680-685.
41. Linstedt A. D., Hauri H. P. Giantin, a novel conserved Golgi membrane protein containing a cytoplasmic domain of at least 350 kDa. Mol. Biol. Cell. 4:1993;679-693.
42. Lippincott-Schwartz J., Cole N. B., Marotta A., Conrad P. A., Bloom G. S. Kinesin is the motor for microtubule-mediated Golgi-to-ER membrane traffic. J. Cell Biol. 128:1995;293-306.
43. Llopis J., McCaffery J. M., Miyawaki A., Farquhar M. G., Tsien R. Y. Measurement of cytosolic, mitochondrial, and Golgi pH in single living cells with green fluorescent proteins. Proc. Natl. Acad. Sci. USA. 95:1998;6803-6808.
44. Lu M., Fritzler M. J., Chan E. K. L. Domains of Golin-97 that mediate its Golgi localization. Mol. Cell. Biol. 9:1998;224a.
45. Mansouri A., Phi-van L., Geithe H. P., Engel W. Proacrosin/acrosin activity during spermiohistogenesis of the bull. Differentiation. 24:1983;149-152.
46. Martinez-Menarguez J. A., Geuze H. J., Ballesta J. Evidence for a nonlysosomal origin of the acrosome. J. Histochem. Cytochem. 44:1996a;313-320.
47. Martinez-Menarguez J. A., Geuze H. J., Ballesta J. Identification of two types of β-COP vesicles in the Golgi complex of rat spermatids. Eur. J. Cell Biol. 71:1996b;137-143.
48. Miller M. G., Mulholland D. J., Vogl A. W. Rat testis motor proteins associated with spermatid translocation (dynein) and spermatid flagella (kinesin II). Biol. Reprod. 60:1999;1047-1056.
49. Mollenhauer H. H., Hass B. S., Morre D. J. Membrane transformation in Golgi apparatus of rat spermatids. J. Microsc. Biol. Cell. 27:1976;33-36.
50. Moreno R. D., Sepúlveda M. S., de Ioannes A., Barros C. The polysulfate binding domain of human proacrosin/acrosin is involved in both the enzyme activation and spermatozoa-zona pellucida interaction. Zygote. 6:1998;75-83.
51. Munro S., Nichols B. J. The GRIP domaina novel Golgi-targeting domain found in several coiled-coil proteins. Curr. Biol. 9:1999;377-380.
52. Nakamura N., Rabouille C., Watson R., Nilsson T., Hui N., Slusarewicz P., Kreis T. E., Warren G. Characterization of a cis-Golgi matrix protein, GM130. J. Cell Biol. 131:1995;1715-1726.
53. Nakamura N., Lowe M., Levine T. P., Rabouille C., Warren G. The vesicle docking protein p115 binds GM130, a cis-Golgi matrix protein, in a mitotically regulated manner. Cell. 89:1997;445-455.
54. Natori S., Huttner W. B. Chromogranin B (secretogranin I) promotes sorting to the regulated secretory pathway of processing intermediates derived from a peptide hormone precursor. Proc. Natl. Acad. Sci. USA. 93:1996;4431-4436.
55. Nichols B. J., Pelham H. R. B. SNAREs and membrane fusion in the Golgi apparatus. Biochim. Biophys. Acta. 1404:1998;9-31.
56. Orci L., Ravazzola M., Amherdt M., Madsen O., Perrelet A., Vassalli J. D., Anderson R. G. Conversion of proinsulin to insulin occurs coordinately with acidification of maturing secretory vesicles. J. Cell Biol. 103:1986;2273-2281.
57. Orci L., Halban P., Perrelet A., Amherdt M., Ravazzola M., Anderson R. G. pH-independent and -dependent cleavage of proinsulin in the same secretory vesicle. J. Cell Biol. 126:1994;1149-1156.
58. Palermo G., Joris H., Devroey P., Van Steirteghem A. C. Pregnancies after intracytoplasmic injection of a single spermatozoon into an oocyte. Lancet. 340:1992;17-18.
59. Peters C., Mayer A. Ca2+/calmodulin signals the completion of docking and triggers a late step of vacuole fusion. Nature. 396:1998;575-580.
60. Russell L. D., Russell J. A., MacGregor G. R., Meistrich M. L. 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. 192:1991;97-120.
61. Santi C. M., Santos T., Hernandez-Cruz A., Darszon A. Properties of a novel pH-dependent Ca2+ permeation pathway present in male germ cells with possible roles in spermatogenesis and mature sperm function. J. Gen. Physiol. 112:1998;33-53.
62. Sasagawa I., Tateno T., Yazawa H., Ichiyanagi O., Ishigooka M., Nakada T. Round spermatids from hybrid sterile mice can initiate normal embryo development. Hum. Reprod. 13:1998;3099-3102.
63. Schulz J. R., Wessel G. M., Vacquier V. D. The exocytosis regulatory proteins syntaxin and VAMP are shed from sea urchin sperm during the acrosome reaction. Dev. Biol. 191:1997;80-87.
64. Schulz J. R., Sasaki J. D., Vacquier V. D. Increased association of synaptosome-associated protein of 25 kDa with syntaxin and vesicle-associated membrane protein following acrosomal exocytosis of sea urchin sperm. J. Biol. Chem. 273:1998;24355-24359.
65. Seelig H. P., Schranz P., Schröter H., Wiemann C., Renz M. MacroGolgin - A new 376 kD Golgi complex outer membrane protein as target of antibodies in patients with rheumatic diseases and HIV infections. J. Autoimmun. 7:1994;67-91.
66. Shima D. T., Cabrera-Poch N., Pepperkok R., Warren G. An ordered inheritance strategy for the Golgi apparatus: Visualization of mitotic disassembly reveals a role for the mitotic spindle. J. Cell Biol. 141:1998;955-966.
67. Sinowatz F., Wrobel K. H. Development of the bovine acrosome. An ultrastructural and cytochemical study. Cell Tissue Res. 219:1981;511-524.
68. Sofikitis N. V., Miyagawa I., Agapitos E., Pasyianos P., Toda T., Hellstrom W. J. G., Kawamura H. Reproductive capacity of the nucleus of the male gamete after completion of meiosis. J. Assit. Reprod. Genet. 11:1994;335-341.
69. Susi F. R., Leblond C. P., Clermont Y. Changes in the Golgi apparatus during spermiogenesis in the rat. Am. J. Anat. 130:1971;251-268.
70. Sutovsky P., Ramalho-Santos J., Moreno R. D., Oko R., Hewitson L., Schatten G. On-stage selection of single round spermatids using a vital, mitochondrion-specific fluorescent probe MitoTracker (TM) and high resolution differential interference contrast microscopy. Hum. Reprod. 14:1999;2301-2312.
71. Tesarik J., Mendoza C., Testart J. Viable embryos from injection of round spermatids into oocytes. N. Engl. J. Med. 333:1995;525.
72. Thomas C. A., Garner D. L., DeJarnette J. M., Marshall C. E. Fluorometric assessments of acrosomal integrity and viability in cryopreserved bovine spermatozoa. Biol. Reprod. 56:1997;991-998.
73. Tooze S. A. Biogenesis of secretory granules in the trans-Golgi network of neuroendocrine and endocrine cells. Biochim. Biophys. Acta. 1404:1998;231-244.
74. Tulsiani D. R. P., Abou-Haila A., Loeser C. R., Pereira B. M. J. The biological and functional significance of the sperm acrosome and acrosomal enzymes in mammalian fertilization. Exp. Cell Res. 240:1998;151-164.
75. Ungermann C., Sato K., Wickner W. Defining the functions of trans-SNARE pairs. Nature. 396:1998;543-548.
76. Vaisberg E. A., Grissom P. M., McIntosh J. R. Mammalian cells express three distinct dynein heavy chains that are localized to different cytoplasmic organelles. J. Cell Biol. 133:1996;831-842.
77. Valdivia M., Yunes R., Melendez J., de Ioannes A. E., Leyton L., Becker M. I., Barros C. Immunolocalization of proacrosin/acrosin in rabbit sperm during acrosome reaction and in spermatozoa recovered from the perivitelline space. Mol. Reprod. Dev. 37:1994;216-222.
78. West A. P., Willison K. R. Brefeldin A and mannose 6-phosphate regulation of acrosomic related vesicular trafficking. Eur. J. Cell Biol. 70:1996;315-321.
79. Westbrook-Case V. A., Winfrey V. P., Olson G. E. Sorting of the domain-specific acrosomal matrix protein AM50 during spermiogenesis in the guinea pig. Dev. Biol. 167:1995;338-349.
80. Whittaker J. R., Bendre H. L. Kinetics of papain-catalyzed hydrolysis of a N-benzoyl-l-arginine ethyl ester and a N-benzoyl-l-argininamide. J. Am. Chem. Soc. 87:1965;2728-2737.
81. Warren G., Malhotra V. The organization of the Golgi apparatus. Curr. Opin. Cell Biol. 10:1998;493-498.
82. Zmuda J. F., Rivas R. J. The Golgi apparatus and the centrosome are localized to the sites of newly emerging axons in cerebellar granule neurons in vitro. Cell Motil. Cytoskel. 41:1998;18-38.