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Microtubule Polarity in the Peripheral Processes of Trigeminal Ganglion Cells: Relevance for the Retrograde Transport of Herpes Simplex Virus

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Microtubule Polarity in the Peripheral Processes of Trigeminal Ganglion Cells: Relevance for the Retrograde Transport of Herpes Simplex Virus The Journal of Neuroscience, January 1994, 14(l): 318325 Microtubule Polarity in the Peripheral Processes of Trigeminal Ganglion Cells: Relevance for the Retrograde Transport of Herpes Simplex Virus Kimberly S. Topp, Lauren B. Meade, and Jennifer H. LaVail Neuroscience Program and Department of Anatomy, University of California San Francisco, San Francisco, California 94143 The directional movement of many cellular organelles in neu- After disruption of the cornea1 epithelium, HSV can invade rons is dependent on polarized microtubules and direction- neuronal processesin the epithelium and stroma. The glyco- specific motor molecules. Microtubules are also thought to protein-rich envelope of the virion is thought to fuse with the mediate the retrograde transport of herpes simplex virus host cell membrane prior to entry of the virus into the cell (see (HSV) in sensory neurons. To define the cellular machinery Roizman and Sears, 1991, for review). The viral capsid and responsible for retrograde axonal transport of HSV, we have some of the associatedtegument proteins are then transported investigated the polarity of microtubules in the peripheral in a retrograde direction by trigeminal nerve axons to their cell axons of trigeminal ganglion neurons. The long ciliary nerves bodies in the ophthalmic division of the trigeminal ganglion. of rabbits were prepared for a standard “hook assay” of Here the HSV may enter a latent state or replicate and be pack- microtubule polarity. Axons in cross-sectioned nerves con- aged in a membrane-bound vesicle destined for transport in an tained microtubules with almost uniform orientation. The fast- anterogradedirection to both the CNS and the peripheral tissues growing, plus ends of these axonal microtubules are located (LaVail et al., 199 1). The bidirectional axonal transport of HSV distal to the cell body and the slow-growing, minus ends are requiresa cytoskeletal framework, energy, and translocator mol- directed centrally. ecules.In addition, directional cueson the capsid and tegument To determine the role played by microtubules in the ret- as well as on the vesicle that contains mature HSV must be rograde transport of HSV in these axons, we injected the specific for retrograde and anterogradetransport, respectively. retrobulbar space of mice with the microtubule-inhibiting Microtubules are thought to play a central role in the transport drugs colchicine, vinblastine, or nocodazole or with the mi- of recycled proteins, vesicles in the endocytic and lysosomal crofilament inhibitor cytochalasin D and 1 d later inoculated systems,and mitochondria from the axon terminal to the soma the cornea with HSV. We found that colchicine, vinblastine, (LaVail and LaVail, 1974; Bisby, 1982). Previous studies in- or nocodazole reduced by 52-87% the amount of virus re- dicate that HSV takes advantage of the host neuron’s natural covered from the ganglion 3 d postinoculation, compared to machinery for retrograde axonal transport, using microtubules vehicle-treated animals. In contrast, cytochalasin D or/3-lum- for translocation from the nerve terminals in the periphery to icolchicine did not significantly reduce the amount of HSV the cell bodies of dorsal root ganglion neurons in rive (Kris- recovered from the ganglion. We conclude that the retro- tenssonet al., 1971). Microtubules and translocator molecules grade axonal transport of HSV from axon endings in the have also been implicated in the transport of HSV from the cornea to the trigeminal ganglion cell bodies requires intact neurites to the cell bodies of dorsal root ganglion cells in vitro microtubules and occurs in a plus-to-minus direction on the (Kristensson et al., 1986). However, no study has yet provided microtubules. Our data are consistent with the hypothesis quantitative evidence of the dependenceof HSV transport on that the retrograde axonal transport of HSV is mediated by intact microtubules in metabolically active neurons. a minus end-directed motor molecule, for example, cyto- Microtubule polarity is establishedduring development ofthe plasmic dynein. neuron and dictates the direction of organelletransport, in con- [Key words: axonal transport, colchicine, vinblastine, no- junction with translocator molecules.The polarity is defined by codazole, cytochalasin, dynein] the kinetics ofassembly and disassemblyofthe tubulin polymer; monomeric tubulin is added and removed at a faster rate at the Recurrent herpes simplex (HSV) infections of the eye are a plus end and at a much slower rate at the minus end of micro- major clinical problem. Episodesof ocular herpes may lead to tubules. The microtubules within neuritesthat extend from mul- cornea1scarring, uveitic glaucoma, uveitic cataract, or retinitis. tipolar neurons in culture are oriented with their plus ends di- rected toward the growth cones (Baas et al., 1989; Baas and Ahmad, 1993). During development the axon maintains this Received Apr. 8. 1993; revised June 30, 1993; accepted July 6, 1993. microtubule orientation. However, microtubules of opposite We are grateful to Dr. Lenore Pereira for her gift of herpes virus and to Mr. polarity are added to dendritic processes.In contrast, unipolar Pedro Paz and Ms. Ann Nomoto for technical support. This work was supported by NIH Grants EY08773 (J.H.L.) and EY06322 (K.S.T.). L.B.M. was supported sensory neuronsdevelop from bipolar neuroblastsin which mi- b; a UCSF Student Research Committee Fellowship. gration of the cell body toward the periphery of the ganglion Correspondence should be addressed to Dr. Kimberly S. Topp, Department of Anatomy, Box 0452, University of California San Francisco, San Francisco, Cal- leads to the formation of a single neurite that is divided into ifornia 94143-0452. peripheral and central processes(Ramon y Cajal, 1952; Stainier Copyright 0 1994 Society for Neuroscience 0270-6474/94/ 1403 18-08$05.00/O and Gilbert, 1991). The Journal of Neuroscience, January 1994, 14(l) 319 The peripheral processes that supply the cornea1 epithelium electron micrographs. Each axon photographed at high magnification are thin, unmyelinated fibers that end as free nerve endings. In was located in the overview prints of the entire nerve to prevent du- addition to their sensory, afferent responses to chemical, me- plication of microtubule counts. Viral inoculation. A total of 97 BALB/c mice 4-5 weeks old were chanical, or thermal stimuli (Rozma and Beuerman, 1982), these used in the experiments. The mice were anesthetized with an intraper- unipolar neurons also serve an efferent role by releasing neu- itoneal injection of Avertin (Lumb, 1963). Fifty microliters of a 1:I ropeptides that mediate local inflammatory responses (Holzer, solution of 1% atropine sulfate, 0.5% proparacaine hydrochloride were 1988; Beckers et al., 1992). The peripheral processes of unipolar applied to each cornea for I5 sec. Corneas were scratched from limbus to limbus in a grid pattern consisting of IO horizontal and IO vertical cells have been assumed to have axonal characteristics, based scratches made with a 25 gauge needle. Subsequently 10’ plaque-forming on their morphology and the absence of MAP2, a high-molec- units (pfu) of F strain HSV type 1 in IO ~1 of minimal essential medium ular-weight protein associated with microtubules in dendrites was applied to each eye. Mice were monitored daily and treated in (HernBndez et al., 1989; Riederer and Barakat-Walter, 1992). accordance with the Society for Neuroscience guidelines for the use of However, there have been no studies to determine whether the animals in neuroscience research. Ilnrnunqfluorescence. To monitor the spread ofthe viral infection and thick peripheral process of a primary sensory neuron maintains to determine the time required for retrograde transport of the virus, the plus end-distal orientation of microtubules characteristic of cryostat sections of eyes and ganglia were immunolluorescently stained axons or develops a mixed microtubule population character- for HSV antigen. Ten mice were inoculated with HSV- I and maintained istic of dendrites (Bass et al., 1988). Knowledge of the polarity for 24, 48, 72, 96, or 120 hr. Mice were killed with an overdose of ethyl ether vapor and perfused through the left ventricle with 0.9% NaCl of the microtubules in these neuronal processes is a prerequisite followed by 4% paraformaldehyde in 100 mM sodium cacodylate buffer, for the prediction of translocator molecules that may function pH 7.4. The trigeminal ganglia, nerves, and eyes were removed as one in the bidirectional transport of HSV. piece and immediately frozen in liquid Freon cooled by liquid nitrogen. The aims of our study were twofold: to determine the polarity In selected animals the corneas were removed, Rattencd. and frozen as whole-mounts. and uniformity of microtubules in the peripheral processes of Eyes and trigeminal ganglia were sectioned at IO pm in a cryostat. trigeminal ganglion cells that innervate the cornea, and to de- Serial sections were collected on Vectabond-treated glass slides (Vector. termine whether treatment of these processes with microtubule- Palo Alto, CA), air dried for 30 min. and rinsed in 100 mM phosphate- disrupting drugs at doses that do not inhibit metabolic activity buffered saline, pH 7.2 (PBS). Sections were immunolabeled with a affects the retrograde transport of HSV. polyclonal rabbit anti-human HSV antibody conjugated to Huorcscein (Accurate Chemicals. Westburv, NY), coverslipped in 9:l glycerol in We demonstrate that the microtubules in the peripheral pro- PBS with 3% n-propyl gallate, and viewed with i-microscope equipped cesses of the rabbit trigeminal ganglion cells are uniformly ori- with epifluorescence optics. Nonspecific staining was prevented by in- ented with the minus ends nearer the nucleus and the plus ends cubating sections with 10% normal goat serum prior to and during the directed toward the axon terminal and that microtubule-de- application of the primary antibody. As a control, WC found no im- munostaining when the primary antibody lo HSV was omitted. polymerizingdrugs selectively inhibit the transport ofHSV from Cytoskrletal-inhibitingdrugs. A total of 72 mice were used in the drug the cornea to the trigeminal ganglion.
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