NEURONAL AND NONNEURONAL EXPRESSION OF NEUROTROPHINS AND THEIR RECEPTORS IN SENSORY AND SYMPATHETIC-GANGLIA SUGGEST NEW INTERCELLULAR TROPHIC INTERACTIONS

Nerve growth factor promotes the survival of populations of sensory an d sympathetic neurons. Although ganglia have been used for classical a ssays of neurotrophin action, knowledge is incomplete regarding the sp atial arrangements through which neurotrophins are delivered to respon sive cells within the ganglia and their attached nerve trunks. Whereas populations of ganglionic neurons may be capable of responding to a p articular neurotrophin in vitro, the spectrum of receptor components a nd neurotrophins expressed by the various neuronal and nonneuronal cel ls comprising the ganglia in adult rats remains to be elucidated in vi vo. Brain-derived neurotrophic factor (BDNF) mRNA was expressed by a p opulation of small to medium sized neurons in all sensory ganglia exce pt in the mesencephalic nucleus of the trigeminal nerve. Interestingly , BDNF immunoreactivity was detected in a more widespread population o f neurons of these ganglia, as well as in scattered satellite cells of both sensory and sympathetic ganglia. These nonneuronal cells also ex pressed mRNA encoding a truncated form of the BDNF receptor, trkB(trun c), and full-length transcripts of trkB appeared to be confined to neu ronal populations. Several other components of neurotrophin receptors (low-affinity neurotrophin receptor, trk, and trkC) were prominently e xpressed by different populations of neuronal cells in sympathetic and sensory ganglia, but they were not detected in nonneuronal cells, Nei ther nerve growth factor nor neurotrophin-3 mRNAs were detected in the se ganglia. Unexpectedly, BDNF and trkB(trunc) expression was detected in oligodendrocytes myelinating the central processes of sensory neur ons. Schwann cells did not express detectable quantities of either ent ity, thereby establishing a dramatic boundary delineated by neurotropk in/neurotrophin receptor expression that coincided with the interface between the oligodendroglia of the central nervous system (CNS) and Sc hwann cells of the peripheral nervous system (PNS). Localization of BD NF expression to an additional population of nonneuronal cells-satelli te cells within sensory and sympathetic ganglia-suggest a more extensi ve role for neurotrophic factors than originally encompassed by the ta rget-derived neurotrophic-factor-concept paradigm. These data support the hypothesis of a possible autocrine or paracrine trophic interactio n between populations of neuronal and nonneuronal cells in the periphe ral nervous system. BDNF expression in oligodendrocytes but not in Sch wann cells at the CNS/PNS junction may provide an additional means of maintaining cell-appropriate connections in the nervous system. (C) 19 95 Wiley-Liss, Inc.