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J. Biol. Chem., Vol. 279, Issue 16, 16377-16387, April 16, 2004

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Vanilloid Receptor 1 Regulates Multiple Calcium Compartments and Contributes to Ca²⁺-induced Ca²⁺ Release in Sensory Neurons^*

László J. Kárai, James T. Russell, Michael J. Iadarola, and Zoltan Oláh¶

From the Neuronal Gene Expression Unit, Pain and Neurosensory Mechanisms Branch, NIDCR, National Institutes of Health, Bethesda, Maryland 20892 and NICHD, National Institutes of Health, Bethesda, Maryland 20892

Vanilloid receptor 1 belongs to the transient receptor potential ion channel family and transduces sensations of noxious heat and inflammatory hyperalgesia in nociceptive neurons. These neurons contain two vanilloid receptor pools, one in the plasma membrane and the other in the endoplasmic reticulum. The present experiments characterize these two pools and their functional significance using calcium imaging and ⁴⁵Ca uptake in stably transfected cells or dorsal root ganglion neurons. The plasma membrane localized receptor is directly activated by vanilloids. The endoplasmic reticulum pool was demonstrated to be independently activated with 20 µM capsaicin or 1.6 µM resiniferatoxin using a bathing solution containing 10 µM Ruthenium Red (to selectively block plasma membrane-localized receptors) and 100 µM EGTA. We also demonstrate an overlap between the endoplasmic reticulum-localized vanilloid receptor regulated stores and thapsigargin-sensitive stores. Direct depletion of calcium via activation of endoplasmic reticulum-localized vanilloid receptor 1 triggered store operated calcium entry. Furthermore, we found that, in the presence of low extracellular calcium (10^-5 M), either 2 µM capsaicin or 0.1 nM-1.6 µM resiniferatoxin caused a pronounced calcium-induced calcium release in either vanilloid receptor-expressing neurons or heterologous expression systems. This phenomenon may allow new insight into how nociceptive neuron function in response to a variety of nociceptive stimuli both acutely and during prolonged nociceptive signaling.

Received for publication, October 2, 2003 , and in revised form, February 12, 2004.

^* This work was supported by the Division of Intramural Research, NIDCR, DHHS, National Institutes of Health. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

^¶ To whom correspondence should be addressed: National Institutes of Health, Bldg. 49, Rm. 1A19, 49 Convent Dr., MSC-4410, Bethesda, MD 20892-4410. Fax: 301-402-0667; E-mail: zoltan.olah{at}nih.gov.

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