Flagellar mitochondrial association of the male-specific Don Juan protein in Drosophila spermatozoa

A. Santel; N. Blumer; M. Kampfer; R. Renkawitz-Pohl

Summary

The Drosophila don juan gene encodes a basic protein (Don Juan protein), which is solely expressed postmeiotically during spermiogenesis in elongated spermatids and in mature sperm. Transgenic expression of a GFP-tagged Don Juan protein (DJ-GFP) in the male germ line showed an association of the fusion protein with the sperm tail. Detailed examination of DJ-GFP localization revealed novel insights into its distinct temporal and spatial distribution along the sperm tail during the last phase of spermatid maturation. Co-localization of DJ-GFP with actin-labeled cysts demonstrated its emergence in elongated spermatids during individualization. Additionally, the endogenous Don Juan protein was detected with epitope-specific antibodies in finally elongated nuclei of spermatids. After completion of nuclear shaping Don Juan is no longer detectable in the sperm heads with the onset of individualization. Mislocalization of the DJ-GFP protein in flagella of a mutant with defective mitochondrial differentiation provides evidence of mitochondrial association of the fusion protein with flagellar mitochondrial arrays. Ectopically expressed DJ-GFP in premeiotic germ cells as well as salivary gland cells confirmed the capability of the fusion protein to associate with mitochondria. Therefore we suppose that Don Juan is a nuclear-encoded, germ-cell specifically expressed mitochondrial protein, which might be involved in the final steps of mitochondrial differentiation within the flagellum.

REFERENCES

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(1996). Axonemal tubulin polyglycylation probed with two monoclonal antibodies: widespread evolutionary distribution, appearance during spermatozoan maturation and possible function in motility. J. Cell Sci 109, 727–738
OpenUrl Abstract/FREE Full Text
1. Cenci G.,
2. Bonaccorsi S.,
3. Pisano C.,
4. Verni F. and
5. Gatti M.
(1994). Chromatin and microtubule organization during premeiotic, meiotic and early postmeiotic stages of Drosophilamelanogaster spermatogenesis. J. Cell Sci 107, 3521–3534
OpenUrl Abstract/FREE Full Text
1. Fabrizio J.,
2. Hime G.,
3. Lemmon S. and
4. Bazinet C.
(1998). Genetic dissection of sperm individualization in Drosophila melanogaster. Development 125, 1833–1843
OpenUrl Abstract
1. Fitch K. and
2. Wakimoto B.
(1998). The paternal effect gene ms(3)sneaky is required for sperm activation and the initiation of embryogenesis in Drosophila melanogaster. Dev. Biol 197, 270–282
OpenUrl CrossRef PubMed Web of Science
1. Hales K. G. and
2. Fuller M. T.
(1997). Developmentally regulated mitochondrial fusion mediated by a conserved, novel, predicted GTPase. Cell 90, 121–129
OpenUrl CrossRef PubMed Web of Science
1. Häusler T.,
2. Stierhof Y.-D.,
3. Blattner J. and
4. Clayton C.
(1997). Conservation of mitochondrial targeting sequence function in mitochondrial and hydrogenosomal proteins from early-branching eukaryotes Crithidia, Trypanosoma and Trichomonas. Eur. J. Cell Biol 73, 240–251
OpenUrl PubMed Web of Science
1. Hennig W.
(1996). Spermatogenesis in Drosophila. Int. J. Dev. Biol 40, 167–176
OpenUrl PubMed
1. Hime G. R.,
2. Brill J. A. and
3. Fuller M. T.
(1996). Assembly of ring canals in the male germ line from structural components of the contractile ring. J. Cell Sci 109, 2779–2788
OpenUrl Abstract/FREE Full Text
1. Johnson L. V.,
2. Walsh M. L. and
3. Chen L. B.
(1980). Localization of mitochondria in living cells with rhodamine 123. Proc. Nat. Acad. Sci. USA 77, 990–994
OpenUrl Abstract/FREE Full Text
1. Kaltschmidt B.,
2. Glätzer K. H.,
3. Michiels F.,
4. Leiss D. and
5. Renkawitz-Pohl R.
(1991). During spermatogenesis1, 2 and3 tubulin are cell type specifically expressed but nevertheless have the potential to coassemble into different microtubular structures. Eur. J. Cell Biol 54, 110–120
OpenUrl PubMed
1. Karr T. L.
(1991). Intracellular sperm/egg interactions in Drosophila: a three dimensional structural analysis of a paternal product in developing egg. Mech. Dev 34, 101–111
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2. Oldfors A.,
3. Garman J. D.,
4. Barsh G. S. and
5. Clayton D. A.
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OpenUrl Abstract/FREE Full Text
1. Maines J. and
2. Wasserman S.
(1998). Regulation and execution of meiosis in Drosophila males. Curr. Top. Dev. Biol 337, 301–332
OpenUrl
1. Megraw T. L. and
2. Chae C. B.
(1993). Functional complementarity between the HMG1-like yeast mitochondrial histone HM and the bacterial histone-like protein HU. J. Biol. Chem 268, 12758–12763
OpenUrl Abstract/FREE Full Text
1. Multigner L.,
2. Gagnon J.,
3. van Dorsselaer A. and
4. Job D.
(1992). Stabilization of sea urchin flagellar microtubules by histone H1. Nature 360, 33–39
OpenUrl CrossRef PubMed
1. Nakai K. and
2. Kanehisa M.
(1992). A knowledge base for predicting localization sites in eukaryotic cells. Genomics 14, 897–911
OpenUrl CrossRef PubMed Web of Science
1. Parisi M. A. and
2. Clayton D. A.
(1991). Similarity of human mitochondrial transcription factor 1 to high mobility group proteins. Science 252, 965–969
OpenUrl Abstract/FREE Full Text
1. Raff E. C.,
2. Fackenthal J. D.,
3. Hutchens J. A.,
4. Hoyle H. D. and
5. Turner F. R.
(1997). Microtubule architecture specified by a-tubulin isoform. Science 275, 70–73
OpenUrl Abstract/FREE Full Text
1. Santel A.,
2. Winhauer T.,
3. Blumer N. and
4. Renkawitz-Pohl R.
(1997). The Drosophiladon juan gene (dj) gene encodes a novel sperm specific protein component characterized by an unusual domain of a repetitive amino acid motif. Mech. Dev 64, 19–30
OpenUrl CrossRef PubMed Web of Science
1. Schäfer M.,
2. Nayernia K.,
3. Engel W. and
4. Schäfer U.
(1995). Translational control in spermatogenesis. Dev. Biol 172, 344–352
OpenUrl CrossRef PubMed Web of Science
1. Thomas J. O. and
2. Wilson C. M.
(1986). Selective radiolabelling and identification of a strong nucleosome binding site on the globular domain of histone H5. EMBO J 5, 3531–3537
OpenUrl PubMed Web of Science
1. Tokuyasu K. T.
(1974). Dynamics of spermiogenesis in Drosophila melanogaster. III. Relation between axoneme and mitochondrial derivatives. Exp. Cell Res 84, 229–250
OpenUrl
1. Tokuyasu K. T.
(1974). Dynamics of spermiogenesis in Drosophila melanogaster. IV. Nuclear transformation. J. Ultrastruct. Res 48, 284–303
OpenUrl CrossRef PubMed Web of Science
1. Tokuyasu K. T.
(1975). Dynamics of spermiogenesis in Drosophila melanogaster. V. Head-tail alignment. J. Ultrastruct. Res 50, 117–129
OpenUrl CrossRef PubMed
1. Tokuyasu K. T.
(1975). Dynamics of spermiogenesis in Drosophila melanogaster. VI. Significance of ‘onion’ nebenkern formation. J. Ultrastruct. Res 53, 93–112
OpenUrl CrossRef PubMed Web of Science
1. Tokuyasu K. T.,
2. Peacock W. J. and
3. Hardy R. W.
(1972). Dynamics of spermiogenesis in Drosophilamelanogaster. I. Individualization process. Z. Zellforsch 124, 479–506
OpenUrl CrossRef PubMed Web of Science
1. Tokuyasu K.T.,
2. Peacock W. J. and
3. Hardy R. W.
(1972). Dynamics ofspermiogenesis in Drosophilamelanogaster. II. Coiling process. Z. Zellforsch 127, 492–525
OpenUrl CrossRef PubMed Web of Science
1. Travis A. J.,
2. Foster J. A.,
3. Rosenbaum N. A.,
4. Visconti P. E.,
5. Gerton G. L.,
6. Kopf G. S. and
7. Moss S. B.
(1998). Targeting of a germ cell-specific type 1 hexokinase lacking a porin-binding domain to the mitochondria as well as to the head and fibrous sheath of murine spermatozoa. Mol. Biol. Cell 9, 263–276
OpenUrl Abstract/FREE Full Text
1. van Doren M.,
2. Williamson A. L. and
3. Lehmann R.
(1998). Regulation of zygotic gene expression in Drosophila primordial germ cells. Curr. Biol 8, 243–246
OpenUrl CrossRef PubMed Web of Science
1. Wolffe A.,
2. Khochbin S. and
3. Dimitrov S.
(1997). What do linker histones do in chromatin?. BioEssays 19, 249–255
OpenUrl CrossRef PubMed Web of Science
1. Wouters-Tyrou D.,
2. Martinage A.,
3. Chevaillier P. and
4. Sautiere P.
(1998). Nuclear basic proteins in spermiogenesis. Biochimie 80, 117–128
OpenUrl PubMed
1. Yang Z.,
2. Gallicano G. I.,
3. Yu Q.-C. and
4. Fuchs E.
(1997). An unexpected localization of basonuclin in the centrosome, mitochondria, and acrosome of developing spermatids. J. Cell Biol 137, 657–669
OpenUrl Abstract/FREE Full Text

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[1] Akhmanova A.,
Miedema K.,
Wang Y.,
van Bruggen M.,
Berden J. H.,
Moudrianakis E. N. and
Hennig W.
(1997). The localization of histone H3.3 in germ line chromatin of Drosophila males as established with a histone H3.3-specific antiserum. Chromosoma 106, 335–347
OpenUrl CrossRef PubMed

[2] Akhmanova A.,

[3] Miedema K.,

[4] Wang Y.,

[5] van Bruggen M.,

[6] Berden J. H.,

[7] Moudrianakis E. N. and

[8] Hennig W.

[9] Brand A. and
Perrimon N.
(1993). Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401–415
OpenUrl Abstract

[10] Brand A. and

[11] Perrimon N.

[12] Bressac C.,
Bre M.-H.,
Darmanaden-Delorme J.,
Laurent M.,
Levilliers N. and
Fleury A.
(1995). A massive new posttranslational modification occurs on axonemal tubulin at the final step of spermatogenesis in Drosophila. Eur. J. Cell Biol 67, 346–355
OpenUrl PubMed

[13] Bressac C.,

[14] Bre M.-H.,

[15] Darmanaden-Delorme J.,

[16] Laurent M.,

[17] Levilliers N. and

[18] Fleury A.

[19] Bre M.-H.,
Redeker V.,
Quibell M.,
Darmanaden-Delorme J.,
Bressac C.,
Cosson J.,
Huitorel P.,
Schmitter J.-M.,
Rossier J.,
Johnson T.,
Adoutte A. and
Levilliers N.
(1996). Axonemal tubulin polyglycylation probed with two monoclonal antibodies: widespread evolutionary distribution, appearance during spermatozoan maturation and possible function in motility. J. Cell Sci 109, 727–738
OpenUrl Abstract/FREE Full Text

[20] Bre M.-H.,

[21] Redeker V.,

[22] Quibell M.,

[23] Darmanaden-Delorme J.,

[24] Bressac C.,

[25] Cosson J.,

[26] Huitorel P.,

[27] Schmitter J.-M.,

[28] Rossier J.,

[29] Johnson T.,

[30] Adoutte A. and

[31] Levilliers N.

[32] Cenci G.,
Bonaccorsi S.,
Pisano C.,
Verni F. and
Gatti M.
(1994). Chromatin and microtubule organization during premeiotic, meiotic and early postmeiotic stages of Drosophilamelanogaster spermatogenesis. J. Cell Sci 107, 3521–3534
OpenUrl Abstract/FREE Full Text

[33] Cenci G.,

[34] Bonaccorsi S.,

[35] Pisano C.,

[36] Verni F. and

[37] Gatti M.

[38] Fabrizio J.,
Hime G.,
Lemmon S. and
Bazinet C.
(1998). Genetic dissection of sperm individualization in Drosophila melanogaster. Development 125, 1833–1843
OpenUrl Abstract

[39] Fabrizio J.,

[40] Hime G.,

[41] Lemmon S. and

[42] Bazinet C.

[43] Fitch K. and
Wakimoto B.
(1998). The paternal effect gene ms(3)sneaky is required for sperm activation and the initiation of embryogenesis in Drosophila melanogaster. Dev. Biol 197, 270–282
OpenUrl CrossRef PubMed Web of Science

[44] Fitch K. and

[45] Wakimoto B.

[46] Hales K. G. and
Fuller M. T.
(1997). Developmentally regulated mitochondrial fusion mediated by a conserved, novel, predicted GTPase. Cell 90, 121–129
OpenUrl CrossRef PubMed Web of Science

[47] Hales K. G. and

[48] Fuller M. T.

[49] Häusler T.,
Stierhof Y.-D.,
Blattner J. and
Clayton C.
(1997). Conservation of mitochondrial targeting sequence function in mitochondrial and hydrogenosomal proteins from early-branching eukaryotes Crithidia, Trypanosoma and Trichomonas. Eur. J. Cell Biol 73, 240–251
OpenUrl PubMed Web of Science

[50] Häusler T.,

[51] Stierhof Y.-D.,

[52] Blattner J. and

[53] Clayton C.

[54] Hennig W.
(1996). Spermatogenesis in Drosophila. Int. J. Dev. Biol 40, 167–176
OpenUrl PubMed

[55] Hennig W.

[56] Hime G. R.,
Brill J. A. and
Fuller M. T.
(1996). Assembly of ring canals in the male germ line from structural components of the contractile ring. J. Cell Sci 109, 2779–2788
OpenUrl Abstract/FREE Full Text

[57] Hime G. R.,

[58] Brill J. A. and

[59] Fuller M. T.

[60] Johnson L. V.,
Walsh M. L. and
Chen L. B.
(1980). Localization of mitochondria in living cells with rhodamine 123. Proc. Nat. Acad. Sci. USA 77, 990–994
OpenUrl Abstract/FREE Full Text

[61] Johnson L. V.,

[62] Walsh M. L. and

[63] Chen L. B.

[64] Kaltschmidt B.,
Glätzer K. H.,
Michiels F.,
Leiss D. and
Renkawitz-Pohl R.
(1991). During spermatogenesis1, 2 and3 tubulin are cell type specifically expressed but nevertheless have the potential to coassemble into different microtubular structures. Eur. J. Cell Biol 54, 110–120
OpenUrl PubMed

[65] Kaltschmidt B.,

[66] Glätzer K. H.,

[67] Michiels F.,

[68] Leiss D. and

[69] Renkawitz-Pohl R.

[70] Karr T. L.
(1991). Intracellular sperm/egg interactions in Drosophila: a three dimensional structural analysis of a paternal product in developing egg. Mech. Dev 34, 101–111
OpenUrl CrossRef PubMed Web of Science

[71] Karr T. L.

[72] Larsson N.-G.,
Oldfors A.,
Garman J. D.,
Barsh G. S. and
Clayton D. A.
(1997). Down-regulation of mitochondrial transcription factor A during spermatogenesis in humans. Hum. Mol. Genet 6, 185–191
OpenUrl Abstract/FREE Full Text

[73] Larsson N.-G.,

[74] Oldfors A.,

[75] Garman J. D.,

[76] Barsh G. S. and

[77] Clayton D. A.

[78] Maines J. and
Wasserman S.
(1998). Regulation and execution of meiosis in Drosophila males. Curr. Top. Dev. Biol 337, 301–332
OpenUrl

[79] Maines J. and

[80] Wasserman S.

[81] Megraw T. L. and
Chae C. B.
(1993). Functional complementarity between the HMG1-like yeast mitochondrial histone HM and the bacterial histone-like protein HU. J. Biol. Chem 268, 12758–12763
OpenUrl Abstract/FREE Full Text

[82] Megraw T. L. and

[83] Chae C. B.

[84] Multigner L.,
Gagnon J.,
van Dorsselaer A. and
Job D.
(1992). Stabilization of sea urchin flagellar microtubules by histone H1. Nature 360, 33–39
OpenUrl CrossRef PubMed

[85] Multigner L.,

[86] Gagnon J.,

[87] van Dorsselaer A. and

[88] Job D.

[89] Nakai K. and
Kanehisa M.
(1992). A knowledge base for predicting localization sites in eukaryotic cells. Genomics 14, 897–911
OpenUrl CrossRef PubMed Web of Science

[90] Nakai K. and

[91] Kanehisa M.

[92] Parisi M. A. and
Clayton D. A.
(1991). Similarity of human mitochondrial transcription factor 1 to high mobility group proteins. Science 252, 965–969
OpenUrl Abstract/FREE Full Text

[93] Parisi M. A. and

[94] Clayton D. A.

[95] Raff E. C.,
Fackenthal J. D.,
Hutchens J. A.,
Hoyle H. D. and
Turner F. R.
(1997). Microtubule architecture specified by a-tubulin isoform. Science 275, 70–73
OpenUrl Abstract/FREE Full Text

[96] Raff E. C.,

[97] Fackenthal J. D.,

[98] Hutchens J. A.,

[99] Hoyle H. D. and

[100] Turner F. R.

[101] Santel A.,
Winhauer T.,
Blumer N. and
Renkawitz-Pohl R.
(1997). The Drosophiladon juan gene (dj) gene encodes a novel sperm specific protein component characterized by an unusual domain of a repetitive amino acid motif. Mech. Dev 64, 19–30
OpenUrl CrossRef PubMed Web of Science

[102] Santel A.,

[103] Winhauer T.,

[104] Blumer N. and

[105] Renkawitz-Pohl R.

[106] Schäfer M.,
Nayernia K.,
Engel W. and
Schäfer U.
(1995). Translational control in spermatogenesis. Dev. Biol 172, 344–352
OpenUrl CrossRef PubMed Web of Science

[107] Schäfer M.,

[108] Nayernia K.,

[109] Engel W. and

[110] Schäfer U.

[111] Thomas J. O. and
Wilson C. M.
(1986). Selective radiolabelling and identification of a strong nucleosome binding site on the globular domain of histone H5. EMBO J 5, 3531–3537
OpenUrl PubMed Web of Science

[112] Thomas J. O. and

[113] Wilson C. M.

[114] Tokuyasu K. T.
(1974). Dynamics of spermiogenesis in Drosophila melanogaster. III. Relation between axoneme and mitochondrial derivatives. Exp. Cell Res 84, 229–250
OpenUrl

[115] Tokuyasu K. T.

[116] Tokuyasu K. T.
(1974). Dynamics of spermiogenesis in Drosophila melanogaster. IV. Nuclear transformation. J. Ultrastruct. Res 48, 284–303
OpenUrl CrossRef PubMed Web of Science

[117] Tokuyasu K. T.

[118] Tokuyasu K. T.
(1975). Dynamics of spermiogenesis in Drosophila melanogaster. V. Head-tail alignment. J. Ultrastruct. Res 50, 117–129
OpenUrl CrossRef PubMed

[119] Tokuyasu K. T.

[120] Tokuyasu K. T.
(1975). Dynamics of spermiogenesis in Drosophila melanogaster. VI. Significance of ‘onion’ nebenkern formation. J. Ultrastruct. Res 53, 93–112
OpenUrl CrossRef PubMed Web of Science

[121] Tokuyasu K. T.

[122] Tokuyasu K. T.,
Peacock W. J. and
Hardy R. W.
(1972). Dynamics of spermiogenesis in Drosophilamelanogaster. I. Individualization process. Z. Zellforsch 124, 479–506
OpenUrl CrossRef PubMed Web of Science

[123] Tokuyasu K. T.,

[124] Peacock W. J. and

[125] Hardy R. W.

[126] Tokuyasu K.T.,
Peacock W. J. and
Hardy R. W.
(1972). Dynamics ofspermiogenesis in Drosophilamelanogaster. II. Coiling process. Z. Zellforsch 127, 492–525
OpenUrl CrossRef PubMed Web of Science

[127] Tokuyasu K.T.,

[128] Peacock W. J. and

[129] Hardy R. W.

[130] Travis A. J.,
Foster J. A.,
Rosenbaum N. A.,
Visconti P. E.,
Gerton G. L.,
Kopf G. S. and
Moss S. B.
(1998). Targeting of a germ cell-specific type 1 hexokinase lacking a porin-binding domain to the mitochondria as well as to the head and fibrous sheath of murine spermatozoa. Mol. Biol. Cell 9, 263–276
OpenUrl Abstract/FREE Full Text

[131] Travis A. J.,

[132] Foster J. A.,

[133] Rosenbaum N. A.,

[134] Visconti P. E.,

[135] Gerton G. L.,

[136] Kopf G. S. and

[137] Moss S. B.

[138] van Doren M.,
Williamson A. L. and
Lehmann R.
(1998). Regulation of zygotic gene expression in Drosophila primordial germ cells. Curr. Biol 8, 243–246
OpenUrl CrossRef PubMed Web of Science

[139] van Doren M.,

[140] Williamson A. L. and

[141] Lehmann R.

[142] Wolffe A.,
Khochbin S. and
Dimitrov S.
(1997). What do linker histones do in chromatin?. BioEssays 19, 249–255
OpenUrl CrossRef PubMed Web of Science

[143] Wolffe A.,

[144] Khochbin S. and

[145] Dimitrov S.

[146] Wouters-Tyrou D.,
Martinage A.,
Chevaillier P. and
Sautiere P.
(1998). Nuclear basic proteins in spermiogenesis. Biochimie 80, 117–128
OpenUrl PubMed

[147] Wouters-Tyrou D.,

[148] Martinage A.,

[149] Chevaillier P. and

[150] Sautiere P.

[151] Yang Z.,
Gallicano G. I.,
Yu Q.-C. and
Fuchs E.
(1997). An unexpected localization of basonuclin in the centrosome, mitochondria, and acrosome of developing spermatids. J. Cell Biol 137, 657–669
OpenUrl Abstract/FREE Full Text

[152] Yang Z.,

[153] Gallicano G. I.,

[154] Yu Q.-C. and

[155] Fuchs E.

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Introducing FocalPlane’s new Community Manager, Esperanza Agullo-Pascual

New funding scheme supports sustainable events

Read & Publish participation continues to grow

Cell scientist to watch: Romain Levayer

Live lactating mammary tissue

JCS and COVID-19

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Summary

REFERENCES

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Related articles

Cited by...

More in this TOC section

Similar articles

Other journals from The Company of Biologists

Introducing FocalPlane’s new Community Manager, Esperanza Agullo-Pascual

New funding scheme supports sustainable events

Read & Publish participation continues to grow

Cell scientist to watch: Romain Levayer

Live lactating mammary tissue

JCS and COVID-19