Contributions of TRPV1, endovanilloids, and endoplasmic reticulum stress in lung cell death in vitro and lung injury

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 302, Issue 1, 2012, Pages

  Thomas, Karen C ^a   Roberts, Jessica K ^a   Deering Rice, Cassandra E ^a   Romero, Erin G ^a   Dull, Randal O ^b   Lee, Jeewoo ^c   Yost, Garold S ^a   Reilly, Christopher A ^a  

^a UNIVERSITY OF UTAH   (United States)

^b UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^c Seoul National University   (South Korea)

Author keywords

Capsaicin; Endovanilloids; Lipopolysaccharides; Lung injury; Transient receptor potential vanilloid 1

Indexed keywords

GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; LACTATE DEHYDROGENASE; LIPOPOLYSACCHARIDE; MESSENGER RNA; NONIVAMIDE; VANILLOID RECEPTOR 1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DEATH; CYTOTOXICITY; ENDOPLASMIC RETICULUM STRESS; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; LUNG ALVEOLUS; LUNG ALVEOLUS CELL; LUNG EDEMA; LUNG INJURY; LUNG LAVAGE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; BRONCHI; BRONCHOALVEOLAR LAVAGE FLUID; CAPSAICIN; CELL DEATH; CELL LINE; CELL LINE, TRANSFORMED; CELLS, CULTURED; ENDOPLASMIC RETICULUM STRESS; HUMANS; INFLAMMATION; L-LACTATE DEHYDROGENASE; LIPOPOLYSACCHARIDES; LUNG; LUNG INJURY; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PULMONARY ALVEOLI; PULMONARY EDEMA; TRANSCRIPTION FACTOR CHOP; TRPV CATION CHANNELS;

EID: 83755184287     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00231.2011     Document Type: Article

References (50)

1. Ang SF, Moochhala SM, Bhatia M. Hydrogen sulfide promotes transient receptor potential vanilloid 1-mediated neurogenic inflammation in polymicrobial sepsis. Crit Care Med 38: 619-628.
2. Bessac BF, Jordt SE. Breathtaking TRP channels: TRPA1 and TRPV1 in airway chemosensation and reflex control. Physiology (Bethesda) 23: 360-370, 2008.
3. Bhatia M, Slavin J, Cao Y, Basbaum AI, Neoptolemos JP. Preprotachykinin-A gene deletion protects mice against acute pancreatitis and associated lung injury. Am J Physiol Gastrointest Liver Physiol 284: G830-G836, 2003.
4. Bhatia M, Wong FL, Fu D, Lau HY, Moochhala SM, Moore PK. Role of hydrogen sulfide in acute pancreatitis and associated lung injury. FASEB J 19: 623-625, 2005.
5. Bhatia M, Zhi L, Zhang H, Ng SW, Moore PK. Role of substance P in hydrogen sulfide-induced pulmonary inflammation in mice. Am J Physiol Lung Cell Mol Physiol 291: L896-L904, 2006.
6. Bottoms GD, Adams HR. Involvement of prostaglandins and leukotrienes in the pathogenesis of endotoxemia and sepsis. J Am Vet Med Assoc 200: 1842-1848, 1992.
7. Caterina MJ, Julius D. The vanilloid receptor: a molecular gateway to the pain pathway. Annu Rev Neurosci 24: 487-517, 2001.
8. Clark N, Keeble J, Fernandes ES, Starr A, Liang L, Sugden D, de Winter P, Brain SD. The transient receptor potential vanilloid 1 (TRPV1) receptor protects against the onset of sepsis after endotoxin. FASEB J 21: 3747-3755, 2007.
9. Collin M, Anuar FB, Murch O, Bhatia M, Moore PK, Thiemermann C. Inhibition of endogenous hydrogen sulfide formation reduces the organ injury caused by endotoxemia. Br J Pharmacol 146: 498-505, 2005.
10. De Petrocellis L, Chu CJ, Moriello AS, Kellner JC, Walker JM, Di Marzo V. Actions of two naturally occurring saturated N-acyldopamines on transient receptor potential vanilloid 1 (TRPV1) channels. Br J Pharmacol 143: 251-256, 2004.
11. De Petrocellis LaDM, V. Lipids as regulators of the activity of transient receptor potential type V1 (TRPV1) channels. Life Sci 77: 1651-1666, 2005.
12. Elekes K, Helyes Z, Nemeth J, Sandor K, Pozsgai G, Kereskai L, Borzsei R, Pinter E, Szabo A, Szolcsanyi J. Role of capsaicin-sensitive afferents and sensory neuropeptides in endotoxin-induced airway inflammation and consequent bronchial hyperreactivity in the mouse. Regul Pept 141: 44-54, 2007.
13. Endo M, Oyadomari S, Suga M, Mori M, Gotoh T. The ER stress pathway involving CHOP is activated in the lungs of LPS-treated mice. J Biochem (Tokyo) 138: 501-507, 2005.
14. Fink MP. Prostaglandins and sepsis: still a fascinating topic despite almost 40 years of research. Am J Physiol Lung Cell Mol Physiol 281: L534-L536, 2001.
15. Fink MP, O'Sullivan BP, Menconi MJ, Wollert PS, Wang H, Youssef ME, Fleisch JH. A novel leukotriene B4-receptor antagonist in endotoxin shock: a prospective, controlled trial in a porcine model. Crit Care Med 21: 1825-1837, 1993.
16. Garami A, Shimansky YP, Pakai E, Oliveira DL, Gavva NR, Romanovsky AA. Contributions of different modes of TRPV1 activation to TRPV1 antagonist-induced hyperthermia. J Neurosci 30: 1435-1440, 2010.
17. Helyes Z, Elekes K, Nemeth J, Pozsgai G, Sandor K, Kereskai L, Borzsei R, Pinter E, Szabo A, Szolcsanyi J. Role of transient receptor potential vanilloid 1 receptors in endotoxin-induced airway inflammation in the mouse. Am J Physiol Lung Cell Mol Physiol 292: L1173-L1181, 2007.
18. Helyes Z, Pinter E, Sandor K, Elekes K, Banvolgyi A, Keszthelyi D, Szoke E, Toth DM, Sandor Z, Kereskai L, Pozsgai G, Allen JP, Emson PC, Markovics A, Szolcsanyi J. Impaired defense mechanism against inflammation, hyperalgesia, and airway hyperreactivity in somatostatin 4 receptor gene-deleted mice. Proc Natl Acad Sci USA 106: 13088-13093, 2009.
19. Hwang SW, Cho H, Kwak J, Lee SY, Kang CJ, Jung J, Cho S, Min KH, Suh YG, Kim D, Oh U. Direct activation of capsaicin receptors by products of lipoxygenases: endogenous capsaicin-like substances. Proc Natl Acad Sci USA 97: 6155-6160, 2000.
20. Kadoi Y, Hinohara H, Kunimoto F, Saito S, Goto F. Cannabinoid antagonist AM 281 reduces mortality rate and neurologic dysfunction after cecal ligation and puncture in rats. Crit Care Med 33: 2629-2636, 2005.
21. Lázár JG, Laxmikant M; Khairathkar-Joshi Neelima M; Blumberg Peter M, Szallasi Arpad. Screening TRPV1 antagonists for the treatment of pain: lessons learned over a decade. Exp Opin Drug Disc 4: 159-180, 2009.
22. Li L, Bhatia M, Zhu YZ, Zhu YC, Ramnath RD, Wang ZJ, Anuar FB, Whiteman M, Salto-Tellez M, Moore PK. Hydrogen sulfide is a novel mediator of lipopolysaccharide-induced inflammation in the mouse. FASEB J 19: 1196-1198, 2005.
23. Maccarrone M, De Petrocellis L, Bari M, Fezza F, Salvati S, Di Marzo V, Finazzi-Agro A. Lipopolysaccharide downregulates fatty acid amide hydrolase expression and increases anandamide levels in human peripheral lymphocytes. Arch Biochem Biophys 393: 321-328, 2001.
24. Matthay MA, Zimmerman GA, Esmon C, Bhattacharya J, Coller B, Doerschuk CM, Floros J, Gimbrone MA Jr, Hoffman E, Hubmayr RD, Leppert M, Matalon S, Munford R, Parsons P, Slutsky AS, Tracey KJ, Ward P, Gail DB, Harabin AL. Future research directions in acute lung injury: summary of a National Heart, Lung, and Blood Institute working group. Am J Respir Crit Care Med 167: 1027-1035, 2003.
25. Matute-Bello M, Ga MA. Animal Models of Acute Lung Injury. ATS Website http://www.thoracic.org/sections/clinical-information/critical-care/ critical-care-research/animal-models-of-acute-lung-injury.html, 2007.
26. Miyamoto R, Otsuguro KI, Ito S. Time-and concentration-dependent activation of TRPA1 by hydrogen sulfide in rat DRG neurons. Neurosci Lett 499: 137-142, 2011.
27. Ng SW, Zhang H, Hegde A, Bhatia M. Role of preprotachykinin-A gene products on multiple organ injury in LPS-induced endotoxemia. J Leukoc Biol 83: 288-295, 2008.
28. Palace GP, Horgan MJ, Malik AB. Generation of 5-lipoxygenase metabolites following pulmonary reperfusion in isolated rabbit lungs. Prostaglandins 43: 339-349, 1992.
29. Puneet P, Hegde A, Ng SW, Lau HY, Lu J, Moochhala SM, Bhatia M. Preprotachykinin-A gene products are key mediators of lung injury in polymicrobial sepsis. J Immunol 176: 3813-3820, 2006.
30. Reilly CA. Neurogenic inflammation: the role of TRP channels in the lung. In: Comprehensive Toxicology, edited by Yost GS. New York, NY: Elsevier, 2010, p. 129-150.
31. Reilly CA, Johansen ME, Lanza DL, Lee J, Lim JO, Yost GS. Calcium-dependent and independent mechanisms of capsaicin receptor (TRPV1)-mediated cytokine production and cell death in human bronchial epithelial cells. J Biochem Mol Toxicol 19: 266-275, 2005.
32. Reilly CA, Taylor JL, Lanza DL, Carr BA, Crouch DJ, Yost GS. Capsaicinoids cause inflammation and epithelial cell death through activation of vanilloid receptors. Toxicol Sci 73: 170-181, 2003.
33. Roche M, Kelly JP, O'Driscoll M, Finn DP. Augmentation of endogenous cannabinoid tone modulates lipopolysaccharide-induced alterations in circulating cytokine levels in rats. Immunology 125: 267-271, 2008.
34. Saghatelian A, McKinney MK, Bandell M, Patapoutian A, Cravatt BF. A FAAH-regulated class of N-acyl taurines that activates TRP ion channels. Biochemistry 45: 9007-9015, 2006.
35. Sio SW, Moochhala S, Lu J, Bhatia M. Early protection from burninduced acute lung injury by deletion of preprotachykinin-A gene. Am J Respir Crit Care Med 181: 36-46, 2000.
36. Sio SW, Puthia MK, Lu J, Moochhala S, Bhatia M. The neuropeptide substance P is a critical mediator of burn-induced acute lung injury. J Immunol 180: 8333-8341, 2008.
37. Streng T, Axelsson HE, Hedlund P, Andersson DA, Jordt SE, Bevan S, Andersson KE, Hogestatt ED, Zygmunt PM. Distribution and function of the hydrogen sulfide-sensitive TRPA1 ion channel in rat urinary bladder. Eur Urol 53: 391-399, 2008.
38. Than M, Nemeth J, Szilvassy Z, Pinter E, Helyes Z, Szolcsanyi J. Systemic anti-inflammatory effect of somatostatin released from capsaicin-sensitive vagal and sciatic sensory fibres of the rat and guinea-pig. Eur J Pharmacol 399: 251-258, 2000.
39. Thomas KC, Ethirajan M, Shahrokh K, Sun H, Lee J, Cheatham TE 3rd, Yost GS, Reilly CA. Structure-activity relationship of capsaicin analogs and transient receptor potential vanilloid 1-mediated human lung epithelial cell toxicity. J Pharmacol Exp Ther 337: 400-410, 2011.
40. Thomas KC, Sabnis AS, Johansen ME, Lanza DL, Moos PJ, Yost GS, Reilly CA. Transient receptor potential vanilloid 1 agonists cause endo-plasmic reticulum stress and cell death in human lung cells. J Pharmacol Exp Ther 321: 830-838, 2007.
41. Trevisani M, Patacchini R, Nicoletti P, Gatti R, Gazzieri D, Lissi N, Zagli G, Creminon C, Geppetti P, Harrison S. Hydrogen sulfide causes vanilloid receptor 1-mediated neurogenic inflammation in the airways. Br J Pharmacol 145: 1123-1131, 2005.
42. Van Der Stelt M, Di Marzo V. Endovanilloids putative endogenous ligands of transient receptor potential vanilloid 1 channels. Eur J Biochem 271: 1827-1834, 2004.
43. Wang Y, Novotny M, Quaiserova-Mocko V, Swain GM, Wang DH. TRPV1-mediated protection against endotoxin-induced hypotension and mortality in rats. Am J Physiol Regul Integr Comp Physiol 294: R1517-R1523, 2008.
44. Ware LB, Matthay MA. The acute respiratory distress syndrome. N Engl J Med 342: 1334-1349, 2000.
45. Wheeler AP, Bernard GR. Acute lung injury and the acute respiratory distress syndrome: a clinical review. Lancet 369: 1553-1564, 2007.
46. Yamaji K, Sarker KP, Kawahara K, Iino S, Yamakuchi M, Abeyama K, Hashiguchi T, Maruyama I. Anandamide induces apoptosis in human endothelial cells: its regulation system and clinical implications. Thromb Haemost 89: 875-884, 2003.
47. Zhang H, Hegde A, Ng SW, Adhikari S, Moochhala SM, Bhatia M. Hydrogen sulfide up-regulates substance p in polymicrobial sepsis-associated lung injury. J Immunol 179: 4153-4160, 2007.
48. Zhang H, Zhi L, Moore PK, Bhatia M. Role of hydrogen sulfide in cecal ligation and puncture-induced sepsis in the mouse. Am J Physiol Lung Cell Mol Physiol 290: L1193-L1201, 2006.
49. Zhang J, Sio SW, Moochhala S, Bhatia M. Role of hydrogen sulfide in severe burn injury-induced inflammation in mice. Mol Med 16: 417-424, 2000.
50. Zygmunt PM, Petersson J, Andersson DA, Chuang H, Sorgard M, Di Marzo V, Julius D, Hogestatt ED. Vanilloid receptors on sensory nerves mediate the vasodilator action of anandamide. Nature 400: 452-457, 1999.