Lamina-associated polypeptide 2 (LAP2) and the thymopoietins (TPs) are a family of proteins described in somatic cells of mammals, which are derived by alternative splicing from a single gene. For one of the members of the family (LAP2 = TPbeta) it has been shown that this integral membrane protein locates to the inner membrane of the nuclear envelope, and that it binds to chromatin and B-type lamins. In the present study, we observed that during the third phase of spermatogenesis (i.e. spermiogenesis), TP-labelling shifted progressively to one half of the nuclear periphery in round spermatids. In the elongating spermatid the signal then becomes restricted to one spot located at the posterior (centriolar) pole of the nucleus. Changes in localization are accompanied by the disappearance, first of TPgamma, and later on of LAP2/TPbeta. TPalpha is the only member of the family detectable in the mature sperm. Concomitantly, lamin B1, the only nuclear lamina protein known to be expressed in mammalian spermatids, showed a similar behaviour, i.e. shifted progressively to the centriolar pole of spermatid nuclei before it became undetectable in fully differentiated mature sperms. These results are the first demonstration that expression and localization patterns of TPs are coordinately and differentially regulated with lamins during a differentiation process.

Alsheimer
M.
,
Benavente
R.
(
1996
).
Change of karyoskeleton during mammalian spermatogenesis: expression pattern of nuclear lamin C2 and its regulation.
Exp. Cell Res
228
,
181
188
Benavente
R.
,
Krohne
G.
(
1985
).
Change of karyoskeleton during spermatogenesis of Xenopus: expression of lamin LIV, a nuclear lamina protein specific for the male germ line.
Proc. Nat. Acad. Sci. USA
82
,
6176
6180
Benavente
R.
,
Krohne
G.
(
1986
).
Involvement of nuclear lamins in postmitotic reorganization of chromatin as demonstrated by microinjection of lamin antibodies.
J. Cell Biol
103
,
1847
1854
Berger
R.
,
Theodor
L.
,
Shoham
J.
,
Gokkel
E.
,
Brok-Simoni
F.
,
Avraham
K. B.
,
Copeland
N. G.
,
Jenkins
N. A.
,
Rechavi
G.
,
Simon
A. J.
(
1996
).
The characterization and localization of the mouse thymopoietin/lamina-associated polypeptide 2 gene and its alternatively spliced products.
Genome Res
6
,
361
370
Collas
P.
,
Poccia
D.
(
1995
).
Lipophilic structures of sperm nuclei target membrane vesicle binding and are incorporated into the nuclear envelope.
Dev. Biol
169
,
123
135
Collas
P.
,
Poccia
D.
(
1996
).
Conserved binding recognition elements of sperm chromatin, sperm lipophilic structures and nuclear envelope precursor vesicles.
Eur. J. Cell Biol
71
,
22
32
Collas
P.
,
Courvalin
J. C.
,
Poccia
D.
(
1996
).
Targeting of membranes to sea urchin sperm chromatin is mediated by a lamin B receptor-like integral membrane protein.
J. Cell Biol
135
,
1715
1725
Cowin
P.
,
Burke
B.
(
1996
).
Cytoskeleton-membrane interactions.
Curr. Opin. Cell Biol
8
,
56
65
Erickson
R. P.
(
1990
).
Post-meiotic gene expression.
Trends Genet
6
,
264
269
Foisner
R.
,
Gerace
L.
(
1993
).
Integral membrane proteins of the nuclear envelope interact with lamins and chromosomes, and binding is modulated by mitotic phosphorylation.
Cell
73
,
1267
1279
Franke
W. W.
,
Schmid
E.
,
Vanderkerckhove
J.
,
Weber
K.
(
1980
).
A permanently proliferating rat vascular smooth cell with maintained expression of smooth muscle characteristics, including actin of the smooth muscle type.
J. Cell Biol
87
,
594
600
Furukawa
K.
,
Hotta
Y.
(
1993
).
cDNA cloning of a germ cell-specific lamin B3 from mouse spermatocytes and analysis of its ectopic expression in somatic cells.
EMBO J
12
,
97
106
Furukawa
K.
,
Inagaki
H.
,
Hotta
Y.
(
1994
).
Identification and cloning of an mRNA coding for a germ cell-specific A-type lamin in mice.
Exp. Cell Res
212
,
426
430
Furukawa
K.
,
Pante
N.
,
Aebi
U.
,
Gerace
L.
(
1995
).
Cloning and cDNA for lamina-associated polypeptide 2 (LAP2) and identification of regions that specify targeting to nuclear envelope.
EMBO J
14
,
1626
1636
Furukawa
K.
,
Fritze
C. E.
,
Gerace
L.
(
1998
).
The major nuclear envelope targeting domain of LAP2 coincides with its lamin binding region but is distinct from its chromatin interaction domain.
J. Biol. Chem
273
,
4213
4219
Georgatos
S.
,
Meier
J.
,
Simons
G.
(
1994
).
Lamins and lamin-associated proteins.
Curr. Opin. Cell Biol
6
,
347
353
Goldberg
M.
,
Jenkins
H.
,
Allen
T.
,
Whitfield
W. G. G.
,
Hutchison
C. J.
(
1995
).
Xenopus lamin B3 has a direct role in the assembly of replication competent nucleus: evidence from cell-free extracts.
J. Cell Sci
108
,
3451
3461
Harris
C. A.
,
Andryuk
P. J.
,
Cline
S. C.
,
Natarajan
A.
,
Siekierka
J. J.
,
Goldstein
G.
(
1994
).
Three distinct human thymopoietins are derived from alternatively spliced mRNAs.
Proc. Nat. Acad. Sci. USA
91
,
6283
6287
Harris
C. A.
,
Andryuk
P. J.
,
Cline
S. C.
,
Mathew
S.
,
Siekierka
J. J.
,
Goldstein
G.
(
1995
).
Structure and mapping of the human thymopoietin (TMPO) gene and relationship of human TMPO to rat lamin-associated polypeptide 2.
Genomics
28
,
198
205
Hecht
N. B.
(
1995
).
The making of a spermatozoon: a molecular perspective.
Dev. Genet
16
,
95
103
Heyting
C.
,
Dietrich
A. J. J.
(
1991
).
Meiotic chromosome preparation and protein labelling.
Meth. Cell Biol
35
,
177
202
Ishijima
Y.
,
Toda
T.
,
Matsuhita
H.
,
Yoshida
M.
,
Kimura
N.
(
1996
).
Expression of thymopoietin/lamina-associated polypeptide 2 (TP /LAP2) and its family proteins as revealed by specific antibody induced against recombinant human thymopoietin.
Biochem. Biophys. Res. Commun
226
,
431
438
Kaufmann
S. H.
(
1989
).
Additional members of the rat lamin polypeptide family. Structural and immunological characterization.
J. Biol. Chem
264
,
13946
13955
Koken
M. H.
,
Hoogerbrugge
J. W.
,
Jasper-Dekker
J.
,
De Wit
J.
,
Willemsen
R.
,
Roest
H. P.
,
Grootegoed
J. A.
,
Hoeijmakers
J. H.
(
1996
).
Expression of the ubiquitin-conjugating DNA repair enzymes HHR6A and B suggests a role in spermatogenesis and chromatin modification.
Dev. Biol
173
,
119
132
Longo
F. J.
,
Krohne
G.
,
Franke
W. W.
(
1987
).
Basic protein of the perinuclear theca of mammalian spermatozoa and spermatids: a novel class of cytoskeletal elements.
J. Cell Biol
105
,
1105
1120
Matsudaira
P. T.
(
1987
).
Sequence from picomole quantities of proteins electroblotted onto polyvinylidene difluoride membranes.
J. Biol. Chem
262
,
10035
10038
Meier
J.
,
Campbell
K. H. S.
,
Ford
C. C.
,
Stick
R.
,
Hutchison
C. J.
(
1991
).
The role of lamin L III in nuclear assembly and DNA replication in cell-free extracts of Xenopus eggs.
J. Cell Sci
98
,
271
279
Meistrich
M. L.
(
1977
).
Separation of spermatogenic cells and nuclei from rodent testes.
Meth. Cell Biol
15
,
15
54
Newport
J. W.
,
Wilson
K. L.
,
Dunphy
W. G.
(
1990
).
A lamin-independent pathway for nuclear envelope assembly.
J. Cell Biol
111
,
2247
2259
Poccia
D.
,
Collas
P.
(
1997
).
Nuclear envelope dynamics during male pronuclear development.
Dev. Growth Differ
39
,
541
550
Rivkin
E.
,
Cullinan
E. B.
,
Tres
L. L.
,
Kierszenbaum
A. L.
(
1997
).
A protein associated with the manchette during rat spermiogenesis is encoded by a gene of the TBP-1-like subfamily with highly conserved ATPase and protease domains.
Mol. Reprod. Dev
48
,
77
89
Smith
A.
,
Benavente
R.
(
1992
).
Identification of a short lamin proteinselectively expressed during meiotic stages of rat spermatogenesis.
Differentiation
52
,
55
60
Smith
A.
,
Benavente
R.
(
1992
).
Identification of a structural protein component of rat synaptonemal complexes.
Exp. Cell Res
198
,
291
297
Spann
T. P.
,
Moir
R. D.
,
Goldman
A. E.
,
Stick
R.
,
Goldman
R. D.
(
1997
).
Disruption of nuclear laming organization alters the distribution of replication factors and inhibits DNA synthesis.
J. Cell Biol
136
,
1201
1212
Thomas
J. O.
,
Kornberg
R. D.
(
1975
).
An octamere of histones in chromatin and free solution.
Proc. Nat. Acad. Sci. USA
72
,
2626
2630
Vester
B.
,
Smith
A.
,
Krohne
G.
,
Benavente
R.
(
1993
).
Presence of a nuclear lamina in pachytene spermatocytes of the rat.
J. Cell Sci
104
,
557
563
Ward
W. S.
,
Partin
A. W.
,
Coffey
D. S.
(
1989
).
DNA loop domains in mammalian spermatozoa.
Chromosoma
98
,
157
159
Wing
S. S.
,
Bedard
N.
,
Morales
C.
,
Hingamp
P.
,
Trasler
J.
(
1996
).
A novel rat homolog of Saccharomyces cerevisiae ubiquitin-conjugating enzymes UBC4 and UBC5 with distinct biochemical features is induced during spermatogenesis.
Mol. Cell. Biol
16
,
4064
4072
Ye
O.
,
Worman
H. J.
(
1996
).
Interaction between an integral protein of the nuclear envelope inner membrane and human chromodomain proteins homologous to Drosophila HP1.
J. Biol. Chem
271
,
14653
14656
Yang
L.
,
Guan
T.
,
Gerace
L.
(
1997
).
Lamin-binding fragment of LAP2 inhibits increase in nuclear volume during the cell cycle and progression into S phase.
J. Cell Biol
139
,
1077
1087
Zalenski
A. O.
,
Allen
M. J.
,
Kobayashi
A.
,
Zalenskaya
I. A.
,
Balhorn
R.
,
Bradbury
E. M.
(
1995
).
Well-defined genome architecture in the human sperm nucleus.
Chromosoma
103
,
577
590
Zalenski
A. O.
,
Tomilin
N. V.
,
Zalenskaya
I. A.
,
Teplitz
R. L.
,
Bradbury
E. B.
(
1997
).
Telomere-telomere interactions and candidate telomere binding protein(s) in mammalian sperm cells.
Exp. Cell Res
232
,
29
41
This content is only available via PDF.