Transient receptor potential vanilloid type 1 channels act as mechanoreceptors and cause substance P release and sensory activation in rat kidneys

American Journal of Physiology - Renal Physiology

Volumn 294, Issue 2, 2008, Pages

  Feng, Nan Hsiung ^a   Lee, Hsang Hsing ^b   Shiang, Jeng Chaun ^a   Ma, Ming Chieh ^c  

^a KAOHSIUNG ARMED FORCES GENERAL HOSPITAL   (Taiwan)

^b CARDINAL TIEN HOSPITAL   (Taiwan)

^c FU JEN CATHOLIC UNIVERSITY   (Taiwan)

Author keywords

Capsaicin receptor; Intrapelvic pressure; Neurokinin 1 receptor; Renorenal reflex

Indexed keywords

2 BENZHYDRYL 3 (2 IODOBENZYLAMINO)QUINUCLIDINE; CAPSAICIN; CAPSAZEPINE; RESINIFERATOXIN; SUBSTANCE P; SUBSTANCE P ANTAGONIST; UNCLASSIFIED DRUG; VANILLOID RECEPTOR 1;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY LABELING; ARTICLE; CONTROLLED STUDY; DIURESIS; ELECTROPHYSIOLOGY; FEMALE; IMMUNOBLOTTING; KIDNEY PELVIS; MECHANORECEPTOR; NATRIURESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; SENSORY NERVE;

EID: 38849207782     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00308.2007     Document Type: Article

References (42)

1. Ahluwalia J, Urban L, Bevan S, Nagy I. Anandamide regulates neuropeptide release from capsaicin-sensitive primary sensory neurons by activating both the cannabinoid 1 receptor and the vanilloid receptor 1 in vitro. Eur J Neurosci 17: 2611-2618, 2003.
2. Avelino A, Cruz C, Nagy I, Cruz F. Vanilloid receptor 1 expression in the rat urinary tract. Neuroscience 109: 787-798, 2002.
3. Birder LA, Nakamura Y, Kiss Nealen ML S, Barrick S, Kanai AJ, Wang E, Ruiz G, De Groat WC, Apodaca G, Watkins S, Caterina MJ. Altered urinary bladder function in mice lacking the vanilloid receptor TRPV1. Nat Neurosci 5: 856-860, 2002.
4. Caterina MJ, Leffler A, Malmberg AB, Martin WJ, Trafton J, Petersen-Zeitz KR, Koltzenburg M, Basbaum AI, Julius D. Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science 288: 306-313, 2000.
5. Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, Julius D. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389: 816-824, 1997.
6. Chen Y, Hoover DB. Autoradiographic localization of NK1 and NK3 tachykinin receptors in rat kidney. Peptides 16: 673-681, 1995.
7. Chien CT, Chien HF, Cheng YJ, Chen CF, Hsu SM. Renal afferent signaling diuretic response is impaired in streptozotocin-induced diabetic rats. Kidney Int 57: 203-214, 2000.
8. Cohen DM. TRPV4 and the mammalian kidney. Pflügers Arch 451: 168-175, 2005.
9. Ferguson M, Bell C. Ultrastructural localization and characterization of sensory nerves in the rat kidney. J Comp Neurol 274: 9-16, 1998.
10. Franco-Cereceda A, Henke H, Lundberg JM, Petermann JB, Hokfelt T, Fischer JA. Calcitonin gene-related peptide (CGRP) in capsaicin-sensitive substance P-immunoreactive sensory neurons in animals and man: distribution and release by capsaicin. Peptides 8: 399-410, 1987.
11. Gilmore JP, Tomomatsu E. Renal mechanoreceptors in nonhuman primates. Am J Physiol Regul Integr Comp Physiol 248: R202-R207, 1985.
12. Gontijo JR, Smith LA, Kopp UC. CGRP activates renal pelvic substance P receptors by retarding substance P metabolism. Hypertension 33: 493-498, 1999.
13. Huang CL. The transient receptor potential superfamily of ion channels. J Am Soc Nephrol 15: 1690-1699, 2004.
14. Huang HS, Chen J, Chen CF, Ma MC. Vitamin E attenuates crystal formation in rat kidneys: roles of renal tubular cell death and crystallization inhibitors. Kidney Int 70: 699-710, 2006.
15. Karai L, Brown DC, Mannes AJ, Connelly ST, Brown J, Gandal M, Wellisch OM, Neubert JK, Olah Z, Iadarola MJ. Deletion of vanilloid receptor 1-expressing primary afferent neurons for pain control. J Clin Invest 113: 1344-1352, 2004.
16. 2+ release in sensory neurons. J Biol Chem 279: 16377-16387, 2004.
17. Kopp UC, Cicha MZ, Farley DM, Smith LA, Dixon BS. Renal substance P-containing neurons and substance P receptors impaired in hypertension. Hypertension 31: 815-822, 1998.
18. Kopp UC, Cicha MZ, Smith LA, Hokfelt T. Nitric oxide modulates renal sensory nerve fibers by mechanisms related to substance P receptor activation. Am J Physiol Regul Integr Comp Physiol 281: R279-R290, 2001.
19. Kopp UC, Cicha MZ, Smith LA. Impaired responsiveness of renal mechanosensory nerves in heart failure: role of endogenous angiotensin. Am J Physiol Regul Integr Comp Physiol 284: R116-R124, 2003.
20. 2, and substance P. Am J Physiol Regul Integr Comp Physiol 278: R937-R946, 2000.
21. Liedtke W, Friedman JM. Abnormal osmotic regulation in trpv4-/-mice. Proc Natl Acad Sci USA 100: 13698-13703, 2003.
22. Liu L, Barajas L. The rat renal nerves during development. Anat Embryol (Berl) 188: 345-361, 1993.
23. Liu M, Liu MC, Magoulas C, Priestley JAV, Willmott NJ. Versatile regulation of cytosolic by vanilloid receptor-1 in rat dorsal root ganglion neurons. J Biol Chem 278: 5462-5472, 2003.
24. Ma MC, Huang HS, Chen CF. Impaired renal sensory responses after unilateral ureteral obstruction in the rat. J Am Soc Nephrol 13: 1008-1016, 2002.
25. Ma MC, Huang HS, Chien CT, Wu MS, Chen CF. Temporal decrease in renal sensory responses in rats after chronic ligation of bile duct. Am J Physiol Renal Physiol 283: F164-F172, 2002.
26. Ma MC, Huang HS, Wu MS, Chien CT, Chen CF. Impaired renal sensory responses after renal ischemia in the rat. J Am Soc Nephrol 13: 1872-1883, 2002.
27. Manzini S, Bacciarelli C, Perfumi M, Massi M. Impairment of renal urinary excretion in neonatal, but not in adult capsaicin-pretreated rats. Neurosci Lett 135: 1-4, 1992.
28. Martinac B. Mechanosensitive ion channels: molecules of mechanotransduction. J Cell Sci 117: 2449-2460, 2004.
29. Olah Z, Szabo T, Karai L, Hough C, Fields RD, Caudle RM, Blumberg PM, Iadarola MJ. Ligand-induced dynamic membrane changes and cell deletion conferred by vanilloid receptor 1. J Biol Chem 276: 11021-11030, 2001.
30. O'Neil RG, Heller S. The mechanosensitive nature of TRPV channels. Pflügers Arch 451: 193-203, 2005.
31. Perfumi M, Massi M. Resiniferatoxin provides further evidence for a role of capsaicin-sensitive sensory neurons in the control of the kidney function. Arch Int Pharmacodyn Ther 327: 232-245, 1994.
32. Schumacher MA, Moff I, Sudanagunta SP, Levine JD. Molecular cloning of an N-terminal splice variant of the capsaicin receptor. Loss of N-terminal domain suggests functional divergence among capsaicin receptor subtypes. J Biol Chem 275: 2756-2762, 2000.
33. Scotland RS, Chauhan S, Davis C, De Felipe C, Hunt S, Kabir J, Kotsonis P, Oh U, Ahluwalia A. Vanilloid receptor TRPV1, sensory C-fibers, and vascular autoregulation: a novel mechanism involved in myogenic constriction. Circ Res 95: 1027-1034, 2004.
34. Stein AT, Ufret-Vincenty CA, Hua L, Santana LF, Gordon SE. Phosphoinositide 3-kinase binds to TRPV1 and mediates NGF-stimulated TRPV1 trafficking to the plasma membrane. J Gen Physiol 128: 509-522, 2006.
35. Suzuki M, Sato J, Kutsuwada K, Ooki G, Imai M. Cloning of a stretch-inhibitable nonselective cation channel. J Biol Chem 274: 6330-6335, 1999.
36. Tian W, Fu Y, Wang DH, Cohen DM. Regulation of TRPV1 by a novel renally expressed rat TRPV1 splice variant. Am J Physiol Renal Physiol 290: F117-F126, 2006.
37. Tominaga M, Caterina MJ, Malmberg AB, Rosen TA, Gilbert H, Skinner K, Raumann BE, Basbaum AI, Julius D. The cloned capsaicin receptor integrates multiple pain-producing stimuli. Neuron 21: 531-543, 1998.
38. Wang DH. The vanilloid receptor and hypertension. Acta Pharmacol Sin 26: 286-294, 2005.
39. Xin H, Tanaka H, Yamaguchi M, Takemori S, Nakamura A, Kohama K. Vanilloid receptor expressed in the sarcoplasmic reticulum of rat skeletal muscle. Biochem Biophys Res Commun 332: 756 -762, 2005.
40. Zhang H, Liu YX, Wu YM, Wang ZM, He RR. Capsaicin facilitates carotid sinus baroreceptor activity in anesthetized rats. Acta Pharmacol Sin 25: 1439-1443, 2004.
41. Zhu Y, Wang Y, Wang DH. Diuresis and natriuresis caused by activation of VR1-positive sensory nerves in renal pelvis of rats. Hypertension 46: 992-997, 2005.
42. Zhuang ZY, Xu H, Clapham DE, Ji RR. Phosphatidylinositol 3-kinase activates ERK in primary sensory neurons and mediates inflammatory heat hyperalgesia through TRPV1 sensitization. J Neurosci 24: 8300-8309, 2004.