The Membrane-Associated Transient Receptor Potential Vanilloid Channel Is the Central Heat Shock Receptor Controlling the Cellular Heat Shock Response in Epithelial Cells

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  Bromberg, Zohar ^a   Goloubinoff, Pierre ^b   Saidi, Younousse ^b   Weiss, Yoram George ^a,c  

^a HEBREW UNIVERSITY   (Israel)

^b UNIVERSITY OF LAUSANNE   (Switzerland)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSAICIN; CAPSAZEPINE; HEAT SHOCK PROTEIN 27; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 90; HEAT SHOCK TRANSCRIPTION FACTOR 1; N (1,4 BENZODIOXAN 6 YL) 3 (4 TERT BUTYLPHENYL)ACRYLAMIDE; RESINIFERATOXIN; SMALL INTERFERING RNA; TRANSIENT RECEPTOR POTENTIAL CHANNEL; TRANSIENT RECEPTOR POTENTIAL CHANNEL 1;

ARTICLE; BIOACCUMULATION; CELL MEMBRANE; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; EMBRYO; EPITHELIUM CELL; HEAT SHOCK RESPONSE; HUMAN; HUMAN CELL; HUMAN TISSUE; INTRACELLULAR SIGNALING; MALE; PROTEIN AGGREGATION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; RNA INTERFERENCE; TRANSCRIPTION INITIATION;

CAPSAICIN; CELL LINE; CELL NUCLEUS; DNA-BINDING PROTEINS; EPITHELIAL CELLS; GENE EXPRESSION REGULATION; HEAT-SHOCK RESPONSE; HSP70 HEAT-SHOCK PROTEINS; HUMANS; PROTEIN BINDING; PROTEIN TRANSPORT; TRANSCRIPTION FACTORS; TRPV CATION CHANNELS;

EID: 84874537340     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0057149     Document Type: Article

References (64)

1. Westerheide SD, Morimoto RI, (2005) Heat shock response modulators as therapeutic tools for diseases of protein conformation. J Biol Chem 280(39): 33097-33100.
2. Kampinga HH, (2006) Chaperones in preventing protein denaturation in living cells and protecting against cellular stress. Handb Exp Pharmacol 72: 1-42.
3. Pratt WB, Toft DO, (2003) Regulation of signaling protein function and trafficking by the hsp90/hsp70-based chaperone machinery. Exp. Biol.Med 228: 111-133.
4. Prahlad V, Cornelius T, Morimoto RI, (2008) Regulation of the Cellular Heat Shock Response in Caenorhabditis elegans by Thermosensory. Neurons Science 320: 811-814.
5. Hinault MP, Farina-Henriquez-Cuendet A, Goloubinoff P, (2011) Molecular Chaperones and Associated Cellular Clearance Mechanisms against Toxic Protein Conformers in Parkinson's Disease. Neurodegener Dis 8(6): 397-412.
6. Bromberg Z, Deutschman CS, Weiss YG, (2005) Heat shock protein 70 and the acute respiratory distress syndrome. J Anesth 19(3): 236-242. Review.
7. Weiss YG, Bromberg Z, Raj N, Raphael J, Goloubinoff P, et al. (2007) Enhanced heat shock protein 70 expression alters proteasomal degradation of IkappaB kinase in experimental acute respiratory distress syndrome. Crit Care Med 35(9): 2128-2138.
8. Bromberg Z, Raj N, Goloubinoff P, Deutschman CS, Weiss YG, (2008) Enhanced Expression of Hsp70 Limits Cell Division in a Sepsis- Induced Model of ARDS. Crit Care Med 36: 246-255.
9. Aschkenasy G, Bromberg Z, Raj N, Deutschman CS, Weiss YG, (2011) Enhanced Hsp70 expression protects the lung during acute lung injury modulating apoptotic cell signaling pathways. PLoS One Vol. 6 (11): e26956.
10. De Los Rios P, Ben-Zvi A, Slutsky O, Azem A, Goloubinoff P, (2006) Hsp70 chaperones accelerate protein translocation and the unfolding of stable protein aggregates by entropic pulling. Proc Natl Acad Sci U S A Apr 18 103(16): 6166-71.
11. Weiss YG, Bouwman A, Gehan B, Schears G, Raj N, et al. (2000) Cecal ligation and double puncture impairs heat shock protein 70 (HSP-70) expression in the lungs of rats. Shock 13(1): 19-23.
12. Tiligada E, (2006) Chemotherapy: induction of stress responses. Endocrin Related Cancer 13: S115-S124.
13. Hohfeld J, (1998) Regulation of the heat shock conjugate Hsc70 in the mammalian cell: the characterization of the anti-apoptotic protein BAG-1 provides novel insights. Biol Chem 379(3): 269-274. Review.
14. Nylandsted J, Rohde M, Brand K, Bastholm L, Elling F, et al. (2000) Selective depletion of heat shock protein 70 (Hsp70) activates a tumor-specific death program that is independent of caspases and bypasses Bcl-2. Proc Natl Acad Sci 97(14): 871-876.
15. Schulte TW, Akinaga S, Soga S, Sullivan W, Stensgard B, et al. (1998) Antibiotic radicicol binds to the N-terminal domain of Hsp90 and shares important biologic activities with geldanamycin. Cell Stress Chaperones 3(2): 100-108.
16. Banerjee, Mustafi S, Chakraborty PK, Raha S, (2010) Modulation of Akt and ERK1/2 pathways by resveratrol in chronic myelogenous leukemia (CML) cells results in the downregulation of Hsp70. PLoS One14 5(1): e8719.
17. Akerfelt M, Morimoto RI, Sistonen L, (2010) Heat shock factors: integrators of cell stress, development and lifespan. Nat Rev Mol Cell Biol Aug 11(8): 545-55.
18. Voellmy R, Boellmann F, (2007) Chaperones regulation of the heat shock protein response. Adv Exp Med Biol 594: 89-99.
19. Akerfelt M, Trouillet D, Mezger V, Sistonen L, (2007) Heat shock factors at crossroad between stress and development. Ann N Y Acad Sci 13: 15-27, review.
20. Trinklein ND, Chen WC, Kingston RE, Myers RM, (2004) Transcriptional regulation and binding of heat shock factor 1 and heat shock factor 2 to 32 human heat shock genes during thermal stress and differentiation. Cell Stress Chaperones 9(1): 21-8.
21. Török Z, Tsvetkova NM, Balogh G, Horváth I, Nagy E, et al. (2003) Heat shock protein coinducers with no effect on protein denaturation specifically modulate the membrane lipid phase. Proc Natl Acad Sci U S A 18 100(6): 3131-6.
22. Balogh G, Horváth I, Nagy E, Hoyk Z, Benkõ S, et al. (2005) The hyperfluidization of mammalian cell membranes acts as a signal to initiate the heat shock protein response. FEBS J272(23): 6077-86.
23. Saidi Y, Finka A, Muriset M, Bromberg Z, Weiss YG, et al. (2009) The heat shock response in moss plants is regulated by specific calcium-permeable channels in the plasma membrane. Plant Cell 21(9): 2829-43.
24. Nagy E, Balogi Z, Gombos I, Akerfelt M, Björkbom A, et al. (2007) Hyperfluidization-coupled membrane microdomain reorganization is linked to activation of the heat shock response in a murine melanoma cell line. Proc Natl Acad Sci U S A 8 104(19): 7945-50.
25. Balogh G, Péter M, Liebisch G, Horváth I, Török Z, et al. (2010) Lipidomics reveals membrane lipid remodelling and release of potential lipid mediators during early stress responses in a murine melanoma cell line. Biochim Biophys Acta 1801(9): 1036-47.
26. Gombos I, Crul T, Piotto S, Güngör B, Török Z, et al. (2011) Membrane-lipid therapy in operation: the HSP co-inducer BGP-15 activates stress signal transduction pathways by remodeling plasma membrane rafts. PLoS One 6(12): e28818.
27. Akiyama H, Sasaki N, Hanazawa S, Gotoh M, Kobayashi S, et al. (2011) Novel sterol glucosyltransferase in the animal tissue and cultured cells: evidence that glucosylceramide as glucose donor. Biochim Biophys Acta 1811(5): 314-22.
28. Mosser DD, Kotzbauer PT, Sarge KD, Morimoto RI, (1990) In vitro activation of heat shock transcription factor DNA-binding by calcium and biochemical conditions that affect protein conformation. Proc Natl Acad Sci U S A May 87(10): 3748-52.
29. Roy A, Mandadi S, Fiamma MN, Rodikova E, Ferguson EV, et al. (2012) Anandamide modulates carotid sinus nerve afferent activity via TRPV1 receptors increasing responses to heat. J Appl Physiol 112(1): 212-24.
30. Klafke JZ, da Silva MA, Trevisan G, Rossato MF, da Silva CR, et al. (2012) Involvement of the glutamatergic system in the nociception induced intrathecally for a TRPA1 agonist in rats. Neuroscience 222: 136-46.
31. Marincsák R, Tóth BI, Czifra G, Márton I, Rédl P, et al. (2009) Increased expression of TRPV1 in squamous cell carcinoma of the human tongue. Oral Dis 15: 328-35.
32. Szallasi A, (2011) New developments in the medicinal chemistry of vanilloid TRPV1 and related receptors. Curr Top Med Chem 11(17): 2116-7.
33. Li WH, Lee YM, Kim JY, Kang S, Kim S, et al. (2007) Transient receptor potential vanilloid-1 mediates heat-shock-induced matrix metalloproteinase-1 expression in human epidermal keratinocytes. J Invest Dermatol 127: 2328-2335.
34. Vos MH, Neelands TR, McDonald HA, Choi W, Kroeger PE, et al. (2006) TRPV1b overexpression negatively regulates TRPV1 responsiveness to capsaicin, heat and low pH in HEK293 cells. J Neurochem Nov 99(4): 1088-102.
35. Czifra G, Varga A, Nyeste K, Marincsák R, Tóth BI, et al. (2009) Increased expressions of cannabinoid receptor-1 and transient receptor potential vanilloid-1 in human prostate carcinoma. J Cancer Res Clin Oncol Apr 135(4): 507-14.
36. Wang Q, Carmichael GG, (2004) Effects of length and location on the cellular response to double-stranded RNA. Microbiol Mol Biol Rev 68(3): 432-52.
37. Walton SP, Wu M, Gredell JA, Chan C, (2010) Designing highly active siRNAs for therapeutic applications. FEBS J277(23): 4806-13.
38. Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, et al. (1997) The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature Oct 23 389(6653): 816-24.
39. Liu AY, Mathur R, Mei N, Langhammer CG, Babiarz B, et al. (2011) Neuroprotective drug riluzole amplifies the heat shock factor 1 (HSF1)- and glutamate transporter 1 (GLT1)-dependent cytoprotective mechanisms for neuronal survival. J Biol Chem 28: 2785-2794.
40. Caterina MJ, Rosen TA, Tominaga M, Brake AJ, Julius D, (1999) A capsaicin-receptor homologue with a high threshold for noxious heat. Nature 398: 436-441.
41. Han P, McDonald HA, Bianchi BR, Kouhen RE, Vos MH, et al. (2007) Capsaicin causes protein synthesis inhibition and microtubule disassembly through TRPV1 activities both on the plasma membrane and intracellular membranes. Biochem Pharmacol May 15 73(10): 1635-45.
42. Kiang JG, (1994) Corticotropin-releasing factor increases [Ca2+]i via receptor-mediated Ca2+ channels in human epidermoid A-431 cells. Eur J Pharmacol Apr 15 267(2): 135-42.
43. Saidi Y, Peter M, Finka A, Cicekli C, Vigh L, (2010) Membrane lipid composition affects plant heat sensing and modulates Ca(2+)-dependent heat shock response. Plant Signal Behav 5(12): 1530-3.
44. Balogh G, Horváth I, Nagy E, Hoyk Z, Benkõ S, et al. (2005) The hyperfluidization of mammalian cell membranes acts as a signal to initiate the heat shock protein response. FEBS J272: 6077-6086.
45. Jung J, Shin JS, Lee SY, Hwang SW, Koo J, et al. (2004) Phosphorylation of vanilloid receptor 1 by Ca2_/calmodulin-dependent kinase II regulates its vanilloid binding. J. Biol. Chem 279: 7048-7054.
46. Carratù L, Franceschelli S, Pardini CL, Kobayashi GS, Horvath I, et al. (1996) Membrane lipid perturbation modifies the set point of the temperature of heat shock response in yeast. Proc Natl Acad Sci U S A Apr 30 93(9): 3870-5.
47. Harwood JL, Maresca B, Vigh L, (1998) Does the membrane's physical state control the expression of heat shock and other genes? Trends Biochem Sci Oct 23('0): 369-74.
48. Vigh L, Horváth I, Maresca B, Harwood JL, (2007) Can the stress protein response be controlled by 'membrane-lipid therapy'? Trends Biochem Sci Aug 32(8): 357-63 Epub 2007 Jul 12.
49. Saidi Y, Finka A, Muriset M, Bromberg Z, Weiss YG, et al. (2009) The heat shock response in moss plants is regulated by specific calcium-permeable channels in the plasma membrane. Plant Cell 21(9): 2829-43.
50. Saidi Y, Finka A, Chakhporanian M, Zryd JP, Schaefer DG, et al. (2005) Controlled expression of recombinant proteins in Physcomitrella patens by a conditional heat-shock promoter: a tool for plant research and biotechnology. Plant Mol Biol 59: 697-711.
51. Tominaga M, Caterina MJ, Malmberg AB, Rosen TA, Gilbert H, et al. (1998) The cloned capsaicin receptor integrates multiple pain-producing stimuli. Neuron Sep 21(3): 531-43.
52. Voets T, Droogmans G, Wissenbach U, Janssens A, Flockerzi V, et al. (2004) The principle of temperature-dependent gating in cold- and heat-sensitive TRP channels. Nature Aug 12 430(7001): 748-54.
53. Vay L, Gu C, McNaughton PC, (2012) The thermo-TRP ion channel family: properties and therapeutic implications. Journal of Pharmacology 165: 787-801.
54. Clark N, Keeble J, Fernandes ES, Starr A, Liang L, et al. (2007) The transient receptor potential vanilloid 1 (TRPV1) receptor protects against the onset of sepsis after endotoxin. FASEB J 21(13): 3747-55.
55. Stangl S, Gehrmann M, Riegger J, Kuhs K, Riederer I, et al. (2011) Targeting membrane heat-shock protein 70 (Hsp70) on tumors by cmHsp70.1 antibody. Proc Natl Acad Sci U S A Jan 11 108(2): 733-8.
56. Holzer P, (2008) The pharmacological challenge to tame the transient receptor potential vanilloid-1 (TRPV1) nocisensor. Br J Pharmacol Dec 155(8): 1145-62. Review.
57. Pratt WB, Morishima Y, Osawa Y, (2008) The Hsp90 chaperone machinery regulates signaling by modulating ligand binding clefts. J Biol Chem 283: 22885-22889.
58. Kiang JG, Gist ID, Tsokos GC, (1999) Biochemical requirements for the expression of heat shock protein 72 kda in human breast cancer MCF-7 cells. Mol Cell Biochem 199(1-2): 179-188.
59. Sánchez AM, Sánchez MG, Malagarie-Cazenave S, Olea N, Díaz-Laviada I, (2006) Induction of apoptosis in prostate tumor PC-3 cells and inhibition of xenograft prostate tumor growth by the vanilloid capsaicin. Apoptosis 11(1): 89-99.
60. Cui X, Yu ZY, Wang W, Zheng YQ, Liu W, et al. (2012) Co-Inhibition of HSP70/HSP90 Synergistically Sensitizes Nasopharyngeal Carcinoma Cells Thermotherapy. Integr Cancer Ther Mar 11(1): 61-7.
61. Calderwood SK, Khaleque MA, Sawyer DB, Ciocca DR, (2006) Heat shock proteins in cancer: chaperones of tumorigenesis. Trends Biochem Sci 31(3): 164-72. Review.
62. Franco-Cereceda A, Rydh M, Lou YP, Dalsgaard CJ, Lundberg JM, (1991) Endothelin as a putative sensory neuropeptide in the guinea-pig: different properties in comparison with calcitonin gene-related peptide. Regul Pept Feb 26 32(3): 253-65.
63. Weiss YG, Tazelaar J, Gehan B, Bouwman A, Christofidou-Solomidou M, et al. (2001) Adenoviral vector transfection into the pulmonary epithelium after cecal ligation and puncture (CLP) in rats. Anesthesiology 95: 974-982.
64. Weiss YG, Maloyan A, Tazelaar J, Raj N, Deutschman CS, (2002) Adenoviral transfer of hsp-70 into pulmonary epithelium improves histology and outcome in experimental acute respiratory distress syndrome. J Clin Invest 110: 801-806.