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Vol. 51, Issue 2, 159-212, June 1999
Molecular Mechanisms of Tumor Promotion Section, Laboratory of
Cellular Carcinogenesis and Tumor Promotion, National Cancer Institute,
Bethesda, Maryland
I. Foreword: A Brief History of a Really "Hot" Aspect of
Pharmacology
II. Introduction
A. Overview
B. Capsaicin: Targets and Actions
C. Early, Indirect Evidence for and against a Vanilloid (Capsaicin)
Receptor VR
III. Direct Evidence for a Vanilloid (Capsaicin) Receptor
A. Specific Binding of resiniferatoxin (RTX), a Naturally Occurring
Ultrapotent Agonist
B. Development of Capsazepine, a Competitive Vanilloid Antagonist
C. Cloning of the First VR, Termed VR1
IV. Anatomical Localization and Tissue Specificity of VRs
A. VRs in Primary Sensory Neurons; Colocalization
with Other Receptors, Neuropeptides, and the Isolectin B4
B. VRs in Vagal (Nodose Ganglion) Neurons
C. VRs in Brain
D. Possible Presence of VRs in Nonneuronal Tissues Such as Mast
Cells and Glia
V. Evidence for Multiple VRs
VI. Biochemical Pharmacology of VRs
A. The Cloned VR Is a Nonselective Cation Channel with a Limited
Selectivity for Calcium
B. Role of Calcium in Modulating VR Functions
C. Where Is the Vanilloid Binding Site on VRs?
D. VR1 Is Activated by Noxious Heat and Low pH (Protons): the VR as
an Integrator of Painful Chemical and Physical Stimuli
E. Ruthenium Red Blocks VRs by an Unknown Mechanism
F. VRs Are Sensitized by Inflammatory Mediators and Proinflammatory
Cytokines
G. Aspirin and Related Drugs May in Part Exert Their Analgesic
Actions by Blocking VRs
H. Proposed Role of Phosphorylation Sites in Modulating VR1
Activity
I. Regulation of VR Expression
J. VRs Are Thiol Proteins Displaying Positive Cooperativity
VII. Requirements for Ligand Recognition by VRs: Typical and Novel
Vanilloids
A. Structure-Activity Relations for Capsaicinoids
B. Structure-Activity Relations for Resiniferanoids for Inducing
Calcium Uptake by Sensory Neurons
C. Differences in Structure-Activity Relationships of Vanilloids
for Receptor Binding and Calcium Uptake
D. Why Is RTX Ultrapotent as a Vanilloid?
E. Novel Vanilloids Lacking 3-Hydroxy 4-methoxyphenyl
(Vanillyl) Functionality
1. Sesquiterpene Unsaturated 1,4-Dialdehydes and Related Bioactive
Terpenoids.
2. Triprenyl Phenols as Vanilloids.
3. Implications of the Discovery of Novel Vanilloids Lacking a
Vanillyl-Like Functionality.
VIII. Vanilloid Mechanisms
A. Excitation by Vanilloids
1. Stimulation of Vanilloid-Sensitive Neurons and Its Consequences.
2. Hyperalgesia and Allodynia Following Vanilloid Administration.
B. Desensitization to Vanilloids
1. Desensitization.
2. Tachyphylaxis.
3. Is Lasting Tachyphylaxis Possible Without Prior Excitation?
4. Impairment of Neuronal Functions after Vanilloid Treatment.
4. Down-Regulation of VRs as a Mechanism of Long-Term
Desensitization to Vanilloids.
6. Messenger Plasticity by Vanilloids as a Novel Mechanism of
Analgesia.
C. Neurotoxicity by Vanilloids
IX. Diverse Biological Actions of Vanilloids; VR-Mediated and
Independent Mechanism
X. Species-Related Differences in Vanilloid Actions
A. Species-Related Differences in VR Expression
B. Species-Related Differences in Expression of Sensory
Neuropeptides and Their Receptors
C. Human VRs
XI. Endogenous Vanilloids: Do They Exist?
XII. Vanilloids in Clinical Practice: Current Uses and Future
Perspectives
A. Counterirritation with Capsaicin
B. Desensitization to Capsaicin
C. Adverse Effects of Topical Capsaicin
D. Novel, Innovative Clinical Uses
E. RTX, an Improved Vanilloid Drug Undergoing Clinical Trials
XIII. Vanilloids: Carcinogens, Anticarcinogens, or Neither?
A. Capsaicin
1. Mutagenesis by Capsaicin.
2. Carcinogenesis by Capsaicin: Animal Experiments.
3. May Culinary Hot Pepper Consumption Be a Risk Factor for Stomach
Cancer in Humans?
4. Capsaicin: A Potential Antitumor Agent?
B. RTX
XIV. Concluding Remarks, Emerging Principles, and Future
Perspectives
Appendix
Acknowledgments
Note Added in Proof.
References
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I. Kissin, C. F. Freitas, and E. L. Bradley Jr Memory of pain: the effect of perineural resiniferatoxin. Anesth. Analg., September 1, 2006; 103(3): 721 - 728. [Abstract] [Full Text] [PDF]
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S.-R. Chen and H.-L. Pan Loss of TRPV1-Expressing Sensory Neurons Reduces Spinal {micro} Opioid Receptors But Paradoxically Potentiates Opioid Analgesia J Neurophysiol, May 1, 2006; 95(5): 3086 - 3096. [Abstract] [Full Text] [PDF]
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M Hartel, F F di Mola, F Selvaggi, G Mascetta, M N Wente, K Felix, N A Giese, U Hinz, P Di Sebastiano, M W Buchler, et al. Vanilloids in pancreatic cancer: potential for chemotherapy and pain management Gut, April 1, 2006; 55(4): 519 - 528. [Abstract] [Full Text] [PDF]
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 A. Mori, S. Lehmann, J. O'Kelly, T. Kumagai, J. C. Desmond, M. Pervan, W. H. McBride, M. Kizaki, and H. P. Koeffler Capsaicin, a Component of Red Peppers, Inhibits the Growth of Androgen-Independent, p53 Mutant Prostate Cancer Cells. Cancer Res., March 15, 2006; 66(6): 3222 - 3229. [Abstract] [Full Text] [PDF]
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S. Maione, T. Bisogno, V. de Novellis, E. Palazzo, L. Cristino, M. Valenti, S. Petrosino, V. Guglielmotti, F. Rossi, and V. D. Marzo Elevation of Endocannabinoid Levels in the Ventrolateral Periaqueductal Grey through Inhibition of Fatty Acid Amide Hydrolase Affects Descending Nociceptive Pathways via Both Cannabinoid Receptor Type 1 and Transient Receptor Potential Vanilloid Type-1 Receptors J. Pharmacol. Exp. Ther., March 1, 2006; 316(3): 969 - 982. [Abstract] [Full Text] [PDF]
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E. Lizanecz, Z. Bagi, E. T. Pasztor, Z. Papp, I. Edes, N. Kedei, P. M. Blumberg, and A. Toth Phosphorylation-Dependent Desensitization by Anandamide of Vanilloid Receptor-1 (TRPV1) Function in Rat Skeletal Muscle Arterioles and in Chinese Hamster Ovary Cells Expressing TRPV1 Mol. Pharmacol., March 1, 2006; 69(3): 1015 - 1023. [Abstract] [Full Text] [PDF]
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Y. Wang and D. H. Wang A Novel Mechanism Contributing to Development of Dahl Salt-Sensitive Hypertension: Role of the Transient Receptor Potential Vanilloid Type 1 Hypertension, March 1, 2006; 47(3): 609 - 614. [Abstract] [Full Text] [PDF]
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F. Wei, K. I. Vadakkan, H. Toyoda, L.-J. Wu, M.-G. Zhao, H. Xu, F. W.F. Shum, Y. H. Jia, and M. Zhuo Calcium Calmodulin-Stimulated Adenylyl Cyclases Contribute to Activation of Extracellular Signal-Regulated Kinase in Spinal Dorsal Horn Neurons in Adult Rats and Mice J. Neurosci., January 18, 2006; 26(3): 851 - 861. [Abstract] [Full Text] [PDF]
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N. R. Gavva, R. Tamir, L. Klionsky, M. H. Norman, J.-C. Louis, K. D. Wild, and J. J. S. Treanor Proton Activation Does Not Alter Antagonist Interaction with the Capsaicin-Binding Pocket of TRPV1 Mol. Pharmacol., December 1, 2005; 68(6): 1524 - 1533. [Abstract] [Full Text] [PDF]
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P. Movahed, B. A. G. Jonsson, B. Birnir, J. A. Wingstrand, T. D. Jorgensen, A. Ermund, O. Sterner, P. M. Zygmunt, and E. D. Hogestatt Endogenous Unsaturated C18 N-Acylethanolamines Are Vanilloid Receptor (TRPV1) Agonists J. Biol. Chem., November 18, 2005; 280(46): 38496 - 38504. [Abstract] [Full Text] [PDF]
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E. Y. Kissin, C. F. Freitas, and I. Kissin The Effects of Intraarticular Resiniferatoxin in Experimental Knee-Joint Arthritis Anesth. Analg., November 1, 2005; 101(5): 1433 - 1439. [Abstract] [Full Text] [PDF]
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I. M Poblete, M. L. Orliac, R. Briones, E. Adler-Graschinsky, and J. P. Huidobro-Toro Anandamide elicits an acute release of nitric oxide through endothelial TRPV1 receptor activation in the rat arterial mesenteric bed J. Physiol., October 15, 2005; 568(2): 539 - 551. [Abstract] [Full Text] [PDF]
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M. Tartas, P. Bouye, A. Koitka, V. Jaquinandi, L. Tan, J. L. Saumet, and P. Abraham Cathodal current-induced vasodilation to single application and the amplified response to repeated application in humans rely on aspirin-sensitive mechanisms J Appl Physiol, October 1, 2005; 99(4): 1538 - 1544. [Abstract] [Full Text] [PDF]
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H. Yamamura, S. Ugawa, T. Ueda, M. Nagao, and S. Shimada Icilin Activates the {delta}-Subunit of the Human Epithelial Na+ Channel Mol. Pharmacol., October 1, 2005; 68(4): 1142 - 1147. [Abstract] [Full Text] [PDF]
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E. D. Hogestatt, B. A. G. Jonsson, A. Ermund, D. A. Andersson, H. Bjork, J. P. Alexander, B. F. Cravatt, A. I. Basbaum, and P. M. Zygmunt Conversion of Acetaminophen to the Bioactive N-Acylphenolamine AM404 via Fatty Acid Amide Hydrolase-dependent Arachidonic Acid Conjugation in the Nervous System J. Biol. Chem., September 9, 2005; 280(36): 31405 - 31412. [Abstract] [Full Text] [PDF]
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M.H. Lee, K.-Y. Yeon, C.-K. Park, H.-Y. Li, Z. Fang, M.S. Kim, S.-Y. Choi, S.J. Lee, S. Lee, K. Park, et al. Eugenol Inhibits Calcium Currents in Dental Afferent Neurons Journal of Dental Research, September 1, 2005; 84(9): 848 - 851. [Abstract] [Full Text] [PDF]
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 N. Frossard, E. Naline, C. Olgart Hoglund, O. Georges, and C. Advenier Nerve growth factor is released by IL-1{beta} and induces hyperresponsiveness of the human isolated bronchus Eur. Respir. J., July 1, 2005; 26(1): 15 - 20. [Abstract] [Full Text] [PDF]
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M. R. Brandt, T. A. Cummons, L. Potestio, S. J. Sukoff, and S. Rosenzweig-Lipson Effects of the N-Methyl-D-aspartate Receptor Antagonist Perzinfotel [EAA-090; [2-(8,9-Dioxo-2,6-diazabicyclo[5.2.0]non-1(7)-en-2-yl)-ethyl]phosphonic Acid] on Chemically Induced Thermal Hypersensitivity J. Pharmacol. Exp. Ther., June 1, 2005; 313(3): 1379 - 1386. [Abstract] [Full Text] [PDF]
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T. Ruan, Y. S. Lin, K.-S. Lin, and Y. R. Kou Sensory transduction of pulmonary reactive oxygen species by capsaicin-sensitive vagal lung afferent fibres in rats J. Physiol., June 1, 2005; 565(2): 563 - 578. [Abstract] [Full Text] [PDF]
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B. Liu, C. Zhang, and F. Qin Functional Recovery from Desensitization of Vanilloid Receptor TRPV1 Requires Resynthesis of Phosphatidylinositol 4,5-Bisphosphate J. Neurosci., May 11, 2005; 25(19): 4835 - 4843. [Abstract] [Full Text] [PDF]
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 I. Ben-Shlomo and A. J. W. Hsueh Three's Company: Two or More Unrelated Receptors Pair with the Same Ligand Mol. Endocrinol., May 1, 2005; 19(5): 1097 - 1109. [Abstract] [Full Text] [PDF]
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P. M. W. Lam, J. McDonald, and D. G. Lambert Characterization and comparison of recombinant human and rat TRPV1 receptors: effects of exo- and endocannabinoids Br. J. Anaesth., May 1, 2005; 94(5): 649 - 656. [Abstract] [Full Text] [PDF]
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X. Wang, R. L. Miyares, and G. P Ahern Oleoylethanolamide excites vagal sensory neurones, induces visceral pain and reduces short-term food intake in mice via capsaicin receptor TRPV1 J. Physiol., April 15, 2005; 564(2): 541 - 547. [Abstract] [Full Text] [PDF]
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D. P. Mohapatra and C. Nau Regulation of Ca2+-dependent Desensitization in the Vanilloid Receptor TRPV1 by Calcineurin and cAMP-dependent Protein Kinase J. Biol. Chem., April 8, 2005; 280(14): 13424 - 13432. [Abstract] [Full Text] [PDF]
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M Domenicali, J Ros, G Fernandez-Varo, P Cejudo-Martin, M Crespo, M Morales-Ruiz, A M Briones, J-M Campistol, V Arroyo, E Vila, et al. Increased anandamide induced relaxation in mesenteric arteries of cirrhotic rats: role of cannabinoid and vanilloid receptors Gut, April 1, 2005; 54(4): 522 - 527. [Abstract] [Full Text] [PDF]
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 E. Bodo, T. Biro, A. Telek, G. Czifra, Z. Griger, B. I. Toth, A. Mescalchin, T. Ito, A. Bettermann, L. Kovacs, et al. A Hot New Twist to Hair Biology: Involvement of Vanilloid Receptor-1 (VR1/TRPV1) Signaling in Human Hair Growth Control Am. J. Pathol., April 1, 2005; 166(4): 985 - 998. [Abstract] [Full Text] [PDF]
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M. Bari, N. Battista, F. Fezza, A. Finazzi-Agro, and M. Maccarrone Lipid Rafts Control Signaling of Type-1 Cannabinoid Receptors in Neuronal Cells: IMPLICATIONS FOR ANANDAMIDE-INDUCED APOPTOSIS J. Biol. Chem., April 1, 2005; 280(13): 12212 - 12220. [Abstract] [Full Text] [PDF]
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M. Tartas, P. Bouye, A. Koitka, S. Durand, Y. Gallois, J. L. Saumet, and P. Abraham Early vasodilator response to anodal current application in human is not impaired by cyclooxygenase-2 blockade Am J Physiol Heart Circ Physiol, April 1, 2005; 288(4): H1668 - H1673. [Abstract] [Full Text] [PDF]
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I. Kissin, N. Davison, and E. L. Bradley Jr Perineural Resiniferatoxin Prevents Hyperalgesia in a Rat Model of Postoperative Pain Anesth. Analg., March 1, 2005; 100(3): 774 - 780. [Abstract] [Full Text] [PDF]
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J. B. Morris, W. S. Wilkie, and D. J. Shusterman Acute Respiratory Responses of the Mouse to Chlorine Toxicol. Sci., February 1, 2005; 83(2): 380 - 387. [Abstract] [Full Text] [PDF]
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Y. Ren, X. Zou, L. Fang, and Q. Lin Sympathetic Modulation of Activity in A{delta}- and C-Primary Nociceptive Afferents After Intradermal Injection of Capsaicin in Rats J Neurophysiol, January 1, 2005; 93(1): 365 - 377. [Abstract] [Full Text] [PDF]
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M. Tominaga Molecular Mechanisms of Trigeminal Nociception and Sensation of Pungency Chem Senses, January 1, 2005; 30(suppl_1): i191 - i192. [Full Text] [PDF]
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S Durand, M Tartas, P Bouye, A Koitka, J. L Saumet, and P Abraham Prostaglandins participate in the late phase of the vascular response to acetylcholine iontophoresis in humans J. Physiol., December 15, 2004; 561(3): 811 - 819. [Abstract] [Full Text] [PDF]
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R. S. Scotland, S. Chauhan, C. Davis, C. De Felipe, S. Hunt, J. Kabir, P. Kotsonis, U. Oh, and A. Ahluwalia Vanilloid Receptor TRPV1, Sensory C-Fibers, and Vascular Autoregulation: A Novel Mechanism Involved in Myogenic Constriction Circ. Res., November 12, 2004; 95(10): 1027 - 1034. [Abstract] [Full Text] [PDF]
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S.-C. Chen, T.-J. Chang, and F.-S. Wu Competitive Inhibition of the Capsaicin Receptor-Mediated Current by Dehydroepiandrosterone in Rat Dorsal Root Ganglion Neurons J. Pharmacol. Exp. Ther., November 1, 2004; 311(2): 529 - 536. [Abstract] [Full Text] [PDF]
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H. Yamamura, S. Ugawa, T. Ueda, M. Nagao, and S. Shimada Capsazepine Is a Novel Activator of the {delta} Subunit of the Human Epithelial Na+ Channel J. Biol. Chem., October 22, 2004; 279(43): 44483 - 44489. [Abstract] [Full Text] [PDF]
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 H.-L. Pan and S.-R. Chen Sensing Tissue Ischemia: Another New Function for Capsaicin Receptors? Circulation, September 28, 2004; 110(13): 1826 - 1831. [Abstract] [Full Text] [PDF]
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 M Trevisani, A Milan, R Gatti, A Zanasi, S Harrison, G Fontana, A H Morice, and P Geppetti Antitussive activity of iodo-resiniferatoxin in guinea pigs Thorax, September 1, 2004; 59(9): 769 - 772. [Abstract] [Full Text] [PDF]
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