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The Journal of Neuroscience, June 15, 2003, 23(12):4793-4797

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BRIEF COMMUNICATION
Calcium Signaling in Single Peripheral Sensory Nerve Terminals

Tony D. Gover,¹ Joseph P. Y. Kao,^1,2,3 and Daniel Weinreich^1,4

¹The Neuroscience Program, University of Maryland, ²Medical Biotechnology Center, University of Maryland Biotechnology Institute, and Departments of ³Physiology and ⁴Pharmacology and Experimental Therapeutics, University of Maryland, School of Medicine, Baltimore, Maryland 21201-1559

Peripheral sensory nerve terminals (PSNTs) have a dual function: reporting normal and abnormal sensations and releasing trophic factors to maintain the structure and function of epithelial cells. Although it is widely considered that intracellular Ca²⁺ plays a critical signaling role for both functions, the role of Ca²⁺ signaling has never been studied in PSNTs, primarily because of their small size and anatomical inaccessibility. Here, using epifluoresence microscopy and a fluorescent Ca²⁺ indicator, we report that action potentials or chemical irritation can elicit transient rises in [Ca²⁺]_i (Ca²⁺ transients) in PSNTs within the corneal epithelium of the rat. In vitro electrical stimulation of the ciliary nerves in the eye, or electrical field stimulation of the cornea, evoked Ca²⁺ transients with a magnitude that was proportional to the number of stimuli applied over the range of 1–10 stimuli. Ca²⁺ transients were significantly blocked by 1 mM lidocaine, 4.1 µM saxitoxin (STX), or L-type Ca²⁺ channel antagonists (1 mM diltiazem or 20 µM nifedipine). The nociceptive agonist capsaicin (1 µM) elicited Ca²⁺ transients in all nerve terminals studied. Capsaicin-evoked Ca²⁺ transients were completely blocked by the vanilloid receptor 1 antagonist capsazepine (100 µM). In contrast, capsaicin-evoked Ca²⁺ transients were not attenuated by preincubation with 4.1 µM STX or 20 µM nifedipine. These findings demonstrate, for the first time, that nerve impulses or chemical stimulation promote Ca²⁺ entry into PSNTs, including nociceptors.

View larger version (57K): [in this window] [in a new window]   Figure 1. Illustration of the branching pattern of A and C fiber nerve terminals within the cornea. A and C fibers course together in the collagenous stromal layer. The nerve plexus in the stromal layer consists of extensively branching A and C fibers. The fibers separate as they turn toward the superficial epithelial layers, where they terminate. Letters in parentheses correspond to the images in Figure 2. Adapted from MacIver and Tanelian (1993).

 

View larger version (94K): [in this window] [in a new window]   Figure 2. Fluorescent labeling of corneal nerve fibers. A–C, Nerve fibers were loaded with tetramethylrhodamine dextran (10 kDa) 24 hr before confocal microscopy. A, Subepithelial nerve plexus lying within the stromal layer. B, Superficial nerve terminals 5 µm below corneal surface. C, Nerve terminals lying deeper within the corneal epithelium. Scale bars: (in A) A, B, 25 µm; C, 50 µm. D, E, Nerve terminals loaded with Oregon Green 488 BAPTA-1 dextran (10 kDa) 24 hr before imaging with a cooled CCD camera. D, Nerve terminals imaged immediately before electrical stimulation. E, Same nerve terminals as in D imaged 1 sec after the start of a train of 10 field stimuli (10 Hz). F, F/F0 trace for a section (marked by arrowheads) of the middle nerve terminal seen in D and E; arrow indicates the start of electrical stimulation. Scale bar: (in E) D, E, 35 µm. For Ca2+ imaging in D—F, 500 msec exposures were collected at 1.67 Hz.

 

Key words: trigeminal primary afferents; eye; cornea; nociceptors; calcium; capsaicin

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Received Dec. 9, 2002; revised Apr. 1, 2003; accepted Apr. 3, 2003.

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