INTRODUCTION
The nucleus of all eukaryotic cells from protozoa to mammals
is delimited by a specialized double membrane, the nuclear
envelope that is perforated by nuclear pore complexes (NPC).
NPCs are the sites at which free diffusion of molecules smaller
than 10 nm in diameter, and regulated trafficking of
macromolecules in and out of the nucleus take place. In
particular, transport of karyophilic proteins from their site of
synthesis in the cytoplasm to their destination in the nucleus
has been shown to occur via a number of signal-mediated
pathways that share common features (Corbett and Silver,
1997; Nigg, 1997). Briefly, karyophilic proteins are endowed
with a nuclear location signal (NLS) that is recognized by a
receptor. The protein/receptor complex is actively transported
through the NPC and, once in the nucleus, the complex
dissociates and the receptor returns to the cytoplasm. There is
heterogeneity both at the level of the NLS and of the specific
receptors that recognize them. The prototypical NLS,
exemplified by the SV40 large T antigen, is a seven amino acid
peptide characterized by a high content of basic amino acids.
A variation of this basic residue-rich NLS is the bipartite-type
NLS originally identified in nucleoplasmin and that consists of
two clusters of basic amino acids, with a high prevalence of
lysines, separated by ten amino acids. A third type of NLS,
termed M9, has been recently identified in the RNA binding
protein hnRNPA1 and bears no similarity to the monopartite
and bipartite NLS (Siomi and Dreyfuss, 1995). The
heterogeneity of the NLS is reflected at the level of the
transport receptors the different NLS interact with. A
heterodimeric receptor consisting of importin α and importin
β (also termed karyopherin α and β) binds to the classical
NLS-bearing proteins and brings them to the transport
apparatus located at the NPC. Importin α binds to the NLS,
whereas importin β mediates binding to the NPC. In contrast,
a single monomeric receptor, termed transportin, binds to M9
and mediates nuclear import of hnRNPA1 (Pollard et al.,
1996). Importin β and transportin are distantly related in
sequence and are members of a superfamily of proteins that are
implicated as nuclear transport receptors. Other essential
components involved in nuclear import of most karyophilic
proteins are the small Ras-related GTP-ase, Ran/TC4, and its
regulatory factors. There is so far only one example of Ran-
independent transport, namely the HIV-1 Vpr protein, which
seems to gain nuclear access by using a pathway distinct from
the basic NLS and M9 pathway (Jenkins et al., 1998).
In addition to the NPC architecture, many components of the
nuclear transport apparatus have been conserved throughout
899 Journal of Cell Science 113, 899-906 (2000)
Printed in Great Britain © The Company of Biologists Limited 2000
JCS1034
In all eukaryotic organisms proteins are targeted to the
nucleus via a receptor-mediated mechanism that requires
a specific nuclear localization sequence (NLS) in the
protein. Little is known about this process in
trypanosomatid protozoa that are considered amongst the
earliest divergent eukaryotes. We have used the green
fluorescent protein (gfp) and β-galactosidase reporters to
identify the NLS of two trypanosomal proteins, namely the
Trypanosoma brucei La protein homologue and histone
H2B of T. cruzi. A monopartite NLS was demonstrated at
the C terminus of the La protein, whereas a bipartite NLS
was identified within the first 40 amino acids of histone
H2B. Treatment of live trypanosomes with poisons of ATP
synthesis resulted in exit of the La NLS-gfp fusion from the
nucleus. Interestingly, this fusion protein accumulated at
several discrete sites in the cytoplasm, rather than
equilibrating between the nucleus and the cytoplasm.
When ATP levels returned to normal, the protein reentered
the nucleus, demonstrating that the process was energy
dependent. Finally, using fusion proteins that localize to
the nucleoplasm or the nucleolus, we identified a
subpopulation of mitotic cells in which the chromosomes
have segregated but the daughter nuclei remain connected
by a thin thread-like structure. We propose that cells
containing this structure represent a late stage in nuclear
division that can be placed after chromosome segregation,
but before completion of karyokinesis.
Key words: Trypanosome, Nuclear protein, NLS, La, H2B
SUMMARY
Import of proteins into the trypanosome nucleus and their distribution at
karyokinesis
Maria A. Marchetti
1
, Christian Tschudi
1
, Helen Kwon
1
, Sandra L. Wolin
2,3
and Elisabetta Ullu
1,2,
*
Departments of
1
Internal Medicine and
2
Cell Biology, and
3
Howard Hughes Medical Institute, Yale University School of Medicine,
PO Box 208022, 333 Cedar Street, New Haven, CT 06520-8022, USA
*Author for correspondence (e-mail: elisabetta.ullu@yale.edu)
Accepted 13 December 1999; published on WWW 14 February 2000