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Endogenous Axoplasmic Proteins and Proteins Containing Nuclear The Journal of Neuroscience, September 1993, 13(g): 4064-4071 Endogenous Axoplasmic Proteins and Proteins Containing Nuclear Localization Signal Sequences Use the Retrograde Axonal Transport/Nuclear Import Pathway in Ap/ysia Neurons Robert Schmied,’ Cheng-Chun Huang,2 Xiao-Ping Zhang,’ Danicia A. Ambron,’ and Richard T. Ambron’ ‘Departments of Anatomy and Cell Biology and “Otolaryngology, College of Physicians and Surgeons of Columbia University, New York, New York 10032 When the nuclear localization signal peptide (sp) of the SV We recently described an intracellular pathway in Aplysia neu- 40 large T antigen was coupled to human serum albumin rons that conveys proteins from the axon periphery through the (HSA), rhodaminated (r), and microinjected into axons of axon to the cell body and then into the nucleus (Ambron et al., Aplysia neurons in vitro, the rHSA-sp was conveyed through 1992). The pathway is formally composed of two processes, the axon to the cell body and then into the nucleus (Ambron retrograde axonal transport and nuclear import. While studies et al., 1992). But since rHSA-sp is an artificial construct, we of the latter have been taken to the molecular level (see reviews needed to determine whether naturally occurring nuclear by Goldfarb, 1989; Garcia-Bustos et al., 199 1; Nigg et al., 199 1; proteins use this pathway. We therefore injected calf thymus Silver, 1991) our knowledge of retrograde axonal transport is histone H-l and Xenopus oocyte nucleoplasmin into axons. rather limited (Vallee and Bloom, 199 1) and derives largely from By 3 hr both were retrogradely transported and targeted into studies of material endocytosed at nerve terminals. The dis- the nucleus, though histone H-l less efficiently than rHSA- covery of this novel pathway allows us to view retrograde trans- sp or nucleoplasmin. In contrast, neither rHSA, nor rHSA port from a very different perspective. We initially assembled conjugated to a peptide with a random distribution of basic a construct consisting of the nuclear localization signal peptide amino acids, was transported or imported. To see if proteins (sp) of the SV-40 large T antigen conjugated to rhodaminated that use the pathway remain intact, we coupled sp to HRP. human serum albumin (rHSA) (Lanford et al., 1986). When When injected into varicosities, the HRP-sp was transported/ injected into varicosities on axons of Aplysia neurons regener- imported to the nucleus, where it was enzymatically active. ating in vitro, the rHSA-sp construct was rapidly transported A key issue was to determine whether endogenous pro- through the axon exclusively in the retrograde direction. Trans- teins use this pathway. Consequently, axoplasm was ex- port could be blocked by nocodazole, implying a dependence truded from Aplysia nerves and the proteins were fraction- on microtubules (Ambron et al., 1992). ated by size. SDS-PAGE and Western blots showed that two The fact that the construct gained access to retrograde trans- fractions contained proteins that were recognized by an af- port from the axoplasm suggested that some soluble axonal finity-purified antibody to sp: fraction 3 included sp83, and molecules mimic the rHSA-sp and use the retrograde transport fraction 4 contained sp75. In addition, these two proteins system to travel back to the cell body. It is significant that the were found in nuclei isolated from neurons. To assess trans- sp provides access to retrograde transport as well as nuclear port, the total proteins in the fractions were rhodaminated import. We base this idea on earlier experiments showing that and injected into varicosities. Fraction 3, but not fraction 4, whereas rHSA-sp was transported/imported, rHSA was neither contained protein that was transported through the axon to transported nor imported, and rHSA coupled to a modified form the nucleus. Collectively, these data indicate that endoge- of sp (msp) was transported and imported inefficiently (Ambron nous proteins, perhaps sp83, use the retrograde transport/ et al., 1992). We now provide direct evidence for the role of the nuclear import pathway. Such proteins could inform the nu- peptide by showing that free sp prevents the transport of rHSA- cleus of events in the periphery as in injury or learning and sp. Thus, we believe that sp is the first signal to be identified memory. that targets a protein for axonal transport. In addition, the ability [Key words: retrograde axonal transport, nuclear import, of sp to inhibit the movement of rHSA-sp implies that retro- axoplasm, signal sequence, Aplysia neurons, nucleoplas- grade transport, like nuclear import (Garcia-Bustos et al., 199 1; min] Nigg et al., 199 1; Silver, 199 l), is a saturable process requiring specific receptors in the axoplasm. Receivea Jan. 14, 1993; revised Apr. 2, 1993; accepted Apr. 13, 1993. While the previous studies broadly defined the pathway, sev- We are grateful to Marilyn Smedman for her excellent technical assistance and eral important issues needed to be addressed. First, rHSA-sp is to Dr. John Pintar for comments on the manuscript. We also thank Drs. Karl an artificial construct in which as many as 20 sp moieties are Feldherr for providing samples of nucleoplasmin, Diane Garsetti for synthesizing attached to a single molecule of HSA. Can naturally occurring the signal peptides, and Sindu Krishna for help with the confocal microscopy. R.S. was supported by Training Grant T32 AG 00189. This work was supported nuclear proteins, which contain internal nuclear localization by NIH Grants NS-22150 and NS-26638. sequences (NLSs), also use this pathway? Here we show that Correspondence should be addressed to Richard T. Ambron, Department of Anatomy and Cell Biology, 1204 Black Building, College of Physicians and Sur- they can. Xenopus oocyte nucleoplasmin, for example, is trans- geons, Columbia University, New York, NY 10032. ported and imported almost as efficiently as rHSA-sp. Second, Copyright 0 1993 Society for Neuroscience 0270-6474/93/134064-08$05.00/O we did not determine whether proteins that use this pathway The Journal of Neuroscience, September 1993, f3(9) 4066 remain intact during transport and import; the movement of examined by fluorescence and bright-field microscopy. Optical sections the rHSA-sp was judged solely by fluorescence. Finally, before through the varicosity, axon, cytoplasm, and nucleus were examined to assess fluorescence. Data were collected only from cells with approxi- we can begin to estimate the significance of the pathway to mately the same amount of fluorescence, and the source of the fluores- neurons, we have to identify the endogenous proteins that use cence was localized by reducing the gain. The noise level was minimized the pathway. Several sp-containing proteins are present in the by averaging, using a Kalman filter, and the image was stored on a Aplysia nervous system (Ambron et al., 1992) and we now show Bernoulli disk. An estimate of the amount of fluorescence in each region was obtained using the AREA program of the MRC 600 image processing that two of these, of 75 and 83 kDa, are present in axoplasm system. Briefly, the fluorescent region of the axon was outlined and and the nucleus. In addition, the 83 kDa polypeptide is in a scanned, yielding an average fluorescence per unit area. This value was fraction of axoplasm that exhibits transport/import after injec- then multiplied by the volume occupied by the fluorescence. The process tion. Thus, the 83 kDa constituent has the properties that one was repeated with the nucleus and the two values were used to compute would expect for a protein that uses the pathway. the percent transport. Images were combined and transferred to a Sony video printer. Horseradish peroxidase cytochemistry. Neurons in vitro were injected with HRP-sp. Three hours later they were fixed, washed, permeabilized Materials and Methods with 0.1% Triton X- 100, and incubated in 0.2% 3,3’-diaminobenzidine Animals. Adult Aplysia caltfornica (100-250 gm), obtained from Mar- (Sigma) in 50 mM Tris-HCI (pH 7.6) with the addition of 0.01% H,O, inus (Long Beach, CA), and juvenile animals, obtained from The Uni- (Graham and Kamovsky, 1966). Noninjected neurons in the same dish versity of Miami School of Marine and Atmospheric Sciences (Miami, had no staining of the nucleus. FL), were maintained in circulating, aerated artificial seawater (Aquar- SDS-PAGE and Western blotting. Proteins were extracted into sample ium Systems, Eastlake, OH) with seaweed as food. buffer containing SDS by heating at 70°C for 20 min. Insoluble material Preparation of the nuclear import signal sequence constructs for in- was removed by centrifugation and the supematant was electrophoresed jection. The SD (Lanford and Butel. 1984) was synthesized and purified on a 10% polyacrylamide gel according to Laemmli (1970). Polypeptides >s described iAmbron et al., 1992). Sp and thelysine/arginine -peptide in the gel were either visualized by silver staining or transferred to (LAP; Calbiochem, La Jolla, CA) were coupled to HSA (Calbiochem) nitrocellulose paper to be probed by an affinity-purified antibody to sp or horseradish peroxidase (type VIA, Sigma, St. Louis, MO) with n-mal- (Ambron et al., 1992). eimido-benzoyl-hydroxy-succinimide (Pierce Chemicals, Rockford, IL) (Goldfarb et al., 1986) and the number of peptides/molecule protein was calculated from the change in migration after SDS-PAGE (Dwor- Results etzky et al., 1988). Calf thymus histone H- 1 (Boehringer-Mannheim, Indianapolis, IN), The sp provides access to the retrograde axonal transport nucleoplasmin (a gift from Dr. C. M. Feldherr, Univ. Florida), HSA- portion of the transport/import pathway LAp, and HSA-sp were reacted with tetramethylrhodamine isothio- Previous studies suggested that the sp is recognized by some cyanate (TRITC) (isomer R, Sigma) (Newmeyer et al., 1986) under identical conditions. The rhodamine:protein ratio in the constructs var- component of the retrograde transport system (Ambron et al., ied from 3.5 to 7.0.
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