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Nerve Growth Factor Regulates Sympathetic Ganglion Cell Morphology and Survival in the Adult Mouse

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Nerve Growth Factor Regulates Sympathetic Ganglion Cell Morphology and Survival in the Adult Mouse The Journal of Neuroscience, July 1990, 70(7): 2412-2419 Nerve Growth Factor Regulates Sympathetic Ganglion Cell Morphology and Survival in the Adult Mouse Kenneth G. Fluit,’ Patricia A. Osborne,* Robert E. Schmidt,3 Eugene M. Johnson, Jr.,2 and William D. Snider’ Departments of ’ Neurology, 2 Pharmacology, and 3 Pathology, Washington University School of Medicine, St. Louis, Missouri 63110 We have investigated the effects of prolonged systemic in- pathetic ganglia, and discontinuation of treatment leads to ul- jections of nerve growth factor (NGF) and its antiserum on timate recovery of sympathetic function (Angeletti et al., 1971 a; the survival and morphology of sympathetic ganglion cells Bjerre et al., 1975b). in adult mice. Using intracellular injections of Lucifer yellow Although NGF dependence is less acute in adult animals, in lightly fixed superior cervical ganglia, we show that total long-term exposure to NGF antibodies in autoimmune animals dendritic lengths of ganglion cells are increased 29% after leads to sub.stantialsympathetic ganglion cell death in animals 2 weeks of NGF treatment. The increased dendritic length with high antibody titers (Gorin and Johnson, 1980; Johnson is characterized by increased branching within the dendritic et al., 1982). Further evidence of continued NGF dependence arborization and not by the addition of new primary den- is the occurrenceof cellular atrophy and decreasesin transmitter drites. In addition, cell soma cross-sectional area was in- enzymes after treatment with specific antisera (Angeletti et al., creased 45%. Conversely, administration of NGF antiserum 197la; Goedert et al., 1978; Otten et al., 1979). Conversely, for 1 month decreased total dendritic length by 33%, de- exogenous administration of NGF in the adult animal results creased ganglion cell body size by 26%, and reduced the in sympathetic target hyperinnervation and increasedtarget levels number of neurons in the ganglion by 25%. After 3 months of neurotransmitter (Bjerre et al., 1975a)and sympathetic gan- of NGF antiserum treatment, the number of neurons in the glion cell hypertrophy (Angeletti et al., 1971 b). Furthermore, ganglion was reduced a total of 41%. NGF antiserum treat- intraventricular infusions of NGF can prevent neuronal atrophy ment for 1 month in aged (22 months old) animals reduced and cell death produced by separation of basal forebrain cho- ganglion cell body size by 21% and cell number by 22%, linergic neurons from their hippocampal target after fimbria- decreases that are comparable to those observed in young fornix lesions(Hefti, 1986; Williams et al., 1986; Kramer, 1987) adult animals. Our results indicate that, even in maturity, and can causeincreases in CAT staining and cellular hypertro- sympathetic ganglion cells remain dependent on NGF for phy of uninjured neurons in the basal forebrain and striatum survival and maintenance of dendritic geometry, and this in adult animals (Hagg et al., 1989; Higgins et al., 1989). dependence continues into old age. An aspect of sympathetic ganglion cell dependenceon NGF that hasnot previously been investigated in adult animals is the Sympathetic ganglion cells, which depend on nerve growth fac- regulation of neuronal morphology. A recently described action tor (NGF) for survival and differentiation during early devel- of exogenously administered NGF is the enhancement of den- opment, are thought to be considerably lessdependent on this dritic arborizations of sympathetic ganglion cells during devel- molecule as development proceeds.In vitro, ganglion cells from opment. Injection of NGF into newborn rats markedly increases animals at early developmental stagescannot survive more than total dendritic length and the number of primary dendrites per 48 hr without NGF in the medium (Chun and Patterson, 1977; ganglion cell (Snider, 1988). Furthermore, experimental manip- Greene, 1977; Martin et al., 1988) whereasthese neurons from ulation of target size in the neonatal period also significantly mature animals may no longer require NGF for survival (John- affects dendritic morphology; creating a larger than normal tar- son, 1983; seealso Lindsay, 1988). Zn vivo, administration of get expands dendritic arborizations and increasesthe number NGF antiserum to newborn animals results in almost complete of primary dendrites, whereascreating a smaller target inhibits destruction of sympathetic ganglia (Levi-Montalcini and Book- normal dendritic development (Voyvodic, 1989). er, 1960; Levi-Montalcini and Angeletti, 1966), and axotomy- The potential sensitivity of the dendrites of mature neurons induced target deprivation of sympathetic ganglion cells in the to NGF is of particular interest becauseit hasbeen demonstrated neonatal period leadsto massivecell death (Hendry and Camp- that the dendritic arborizations of rodent sympathetic ganglion bell, 1976). However, after 3 weeks of age, NGF antiserum cells undergo considerable growth and rearrangement in ma- treatment results in less extensive destructive effects on sym- turity (Purves and Hadley, 1985; Purves et al., 1986a;Voyvodic, 1987). Furthermore, axotomy of sympathetic postganglionic fi- Received Feb. 5, 1990; revised March 26, 1990; accepted April 2, 1990. bers in adult mice results in decreasesin ganglion cell cross- This work was supported by NIH grants to W.D.S., E.M.J., and R.E.S. We sectional area and total dendritic length. Reinnervation of the thank P. Amargo, J. Colombo, and S. Plurad for technical assistance. target, however, soon brings these parameters back to control Correspondence should be addressed to Dr. William D. Snider, Department of Neurology, Washington University School of Medicine, Box 8 111, 660 South levels (Yawo, 1987). Theseexperiments suggesta role for target- Euclid Avenue, St. Louis, MO 63 110. derived neurotrophic factors in the regulation of the dendritic Copyright 0 1990 Society for Neuroscience 0270-6474/90/072412-08$03.00/O arborizations of sympathetic ganglion cells, even in adult ani- The Journal of Neuroscience, July 19% f@i’) 2413 mals. Since NGF is known to affect dendritic arborization during of the dendrites were brightly fluorescent as visualized with an epiflu- development, it is a natural candidate to regulate these changes orescence filter for Lucifer yellow (Leitz 12/3 cube). Selection of ganglion cells for intracellular filling was performed by in maturity. focusing down on the surface of the ganglion at the outset of the ex- In this study, we have performed a detailed investigation of periment and impaling the cell that fell under the cross-hairs in the the responseof sympathetic ganglion cells in mature mice to ocular of the microscope. Subsequent cell selections were made by mov- NGF deprivation or administration of exogenous NGF. We ing the microscope stage so that the soma and distal processes of the have chosen to study sympathetic ganglion cells becausethey previously injected cell were completely removed from the field. The ganglion cell on which the cross-hairs fell was the next cell selected for are susceptibleto the effects of systemically administered NGF impalement. By using this technique, S-10 cells per ganglion could be or NGF antiserum. Furthermore, their accessibility for intra- iniected intracellularly without overlap of their dendritic processes and cellular staining permits investigation of the responsesof their without selection bias on the part of the investigator. dendritic arborizations to NGF or anti-NGF treatment. Finally, After intracellular filling, the ganglia were postfixed in 4% parafor- maldehyde at 4°C for 2-3 hr. After fixation the ganglia were dehydrated the number of cells within a ganglion can be counted directly through a graded series of ethanol, cleared in xylene, and coverslipped without the necessityfor specific enzyme (Hefti, 1986; Williams with Krvstalon (Harleco). The cells in the whole mount urenarations et al., 1986; Kramer, 1987) or receptor staining (Richardson et were viewed under fluorescein epifluorescence, photographed, and traced al., 1986; Taniuchi et al., 1986), techniquesnecessary to identify on black paper with a white pencil by using a Leitz 50 x water immersion NGF-dependent populations of neurons within the central ner- objective (NA 1.00) and a camera lucida drawing tube attachment. Dendrites and axons were identified as previously described (Snider, vous system. 1988); dendrites contained secondary and tertiary branches whereas axons were smooth, unbranched processes that could be followed for Materials and Methods several hundred microns until thev exited in the postnanalionic trunks. NGF and anti-NGF treatment. Mouse 2.5s NGF was purified from Cells were rejected from the analysis if the axon could not be followed male mouse submandibular glands according to the method of Bocchini for at least 100 pm. and Angeletti (1969) dissolved in phosphate-buffered saline (0.1 M, pH Several quantitative measures of dendritic morphology were deter- 7.4), and administered daily to young adult female mice (CFl strain, mined. The number of primary dendrites was obtained by viewing the 20-25 gm, 6-8 weeks old, Charles River Laboratories) by subcutaneous cell at 500 x in multiple focal planes. A primary dendrite was identified injection in a dosage of 5 mg/kg. A comparable dose is known to increase as a dendritic process that arose from the ganglion cell soma and ex- sympathetic ganglion cell size, enhance transmitter enzyme synthesis, tended a distance greater than the diameter of the cell soma. Total and enhance
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