Hypoxia-inducible factor 1 regulates heat and cold pain sensitivity and persistence

Antioxidants and Redox Signaling

Volumn 20, Issue 16, 2014, Pages 2555-2571

  Kanngiesser, Maike ^a   Mair, Norbert ^b   Lim, Hee Young ^a   Zschiebsch, Katja ^a   Blees, Johanna ^c   Häussler, Annett ^a   Brüne, Bernhard ^c   Ferreiròs, Nerea ^a   Kress, Michaela ^b   Tegeder, Irmgard ^a  

^a UNIVERSITY HOSPITAL FRANKFURT   (Germany)

^b UNIVERSITY OF INNSBRUCK   (Austria)

^c GOETHE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSAICIN; FORMALDEHYDE; HYPOXIA INDUCIBLE FACTOR 1; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MESSENGER RNA; PROTEIN C FOS; TRANSIENT RECEPTOR POTENTIAL CHANNEL;

ALLODYNIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CALCIUM TRANSPORT; CHRONIC PAIN; COLD; CONTROLLED STUDY; FEMALE; FORMALIN TEST; GENE CONTROL; HEAT; HYPERALGESIA; MALE; MOUSE; NEUROPATHIC PAIN; NOCICEPTION; NONHUMAN; PAIN THRESHOLD; PERCEPTIVE THRESHOLD; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SCIATIC NERVE INJURY; SENSORY NERVE CELL; SPINAL CORD DORSAL HORN; UPREGULATION; ANIMAL; DEFICIENCY; KNOCKOUT MOUSE; METABOLISM;

ANIMALS; COLD TEMPERATURE; FEMALE; HOT TEMPERATURE; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MALE; MICE; MICE, KNOCKOUT; PAIN THRESHOLD;

EID: 84900401376     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2013.5494     Document Type: Article

References (62)

1. Agarwal N, Offermanns S, and Kuner R. Conditional gene deletion in primary nociceptive neurons of trigeminal ganglia and dorsal root ganglia. Genesis 38: 122-129, 2004.
2. Agarwal N, Pacher P, Tegeder I, Amaya F, Constantin CE, Brenner GJ, Rubino T, Michalski CW, Marsicano G, Monory K, Mackie K, Marian C, Batkai S, Parolaro D, Fischer MJ, Reeh P, Kunos G, Kress M, Lutz B, Woolf CJ, and Kuner R. Cannabinoids mediate analgesia largely via peripheral type 1 cannabinoid receptors in nociceptors. Nat Neurosci 10: 870-879, 2007.
3. Baranova O, Miranda LF, Pichiule P, Dragatsis I, Johnson RS, and Chavez JC. Neuron-specific inactivation of the hypoxia inducible factor 1 alpha increases brain injury in a mouse model of transient focal cerebral ischemia. J Neurosci 27: 6320-6332, 2007.
4. Barriere DA, Rieusset J, Chanteranne D, Busserolles J, Chauvin MA, Chapuis L, Salles J, Dubray C, and Morio B. Paclitaxel therapy potentiates cold hyperalgesia in strepto-zotocin-induced diabetic rats through enhanced mitochon-drial reactive oxygen species production and TRPA1 sensitization. Pain 153: 553-561, 2012.
5. Bautista DM, Movahed P, Hinman A, Axelsson HE, Sterner O, Hogestatt ED, Julius D, Jordt SE, and Zygmunt PM. Pungent products from garlic activate the sensory ion channel TRPA1. Proc Natl Acad Sci USA 102: 12248-12252, 2005.
6. Bockhart V, Constantin CE, Haussler A, Wijnvoord N, Kanngiesser M, Myrczek T, Pickert G, Popp L, Sobotzik JM, Pasparakis M, Kuner R, Geisslinger G, Schultz C, Kress M, and Tegeder I. Inhibitor kappaB Kinase beta deficiency in primary nociceptive neurons increases TRP channel sensitivity. J Neurosci 29: 12919-12929, 2009.
7. Brune B and Zhou J. The role of nitric oxide (NO) in stability regulation of hypoxia inducible factor-1alpha (HIF-1alpha). Curr Med Chem 10: 845-855, 2003.
8. Bull R, Finkelstein JP, Galvez J, Sanchez G, Donoso P, Behrens MI, and Hidalgo C. Ischemia enhances activation by Ca2+ and redox modification of ryanodine receptor channels from rat brain cortex. J Neurosci 28: 9463-9472, 2008.
9. Campbell CM, Edwards RR, Carmona C, Uhart M, Wand G, Carteret A, Kim YK, Frost J, and Campbell JN. Polymorphisms in the GTP cyclohydrolase gene (GCH1) are associated with ratings of capsaicin pain. Pain 141: 114-118, 2009.
10. Chattopadhyay M, Walter C, Mata M, and Fink DJ. Neuroprotective effect of herpes simplex virus-mediated gene transfer of erythropoietin in hyperglycemic dorsal root ganglion neurons. Brain 132: 879-888, 2009.
11. Cheng LZ, Lu N, Zhang YQ, and Zhao ZQ. Ryanodine receptors contribute to the induction of nociceptive input-evoked long-term potentiation in the rat spinal cord slice. Mol Pain 6: 1, 2010.
12. Decosterd I and Woolf CJ. Spared nerve injury: an animal model of persistent peripheral neuropathic pain. Pain 87: 149-158, 2000.
13. Diebold I, Petry A, Hess J, and Gorlach A. The NADPH oxidase subunit NOX4 is a new target gene of the hypoxia-inducible factor-1. Mol Biol Cell 21: 2087-2096, 2010.
14. Digicaylioglu M and Lipton SA. Erythropoietin-mediated neuroprotection involves cross-talk between Jak2 and NF-kappaB signalling cascades. Nature 412: 641-647, 2001.
15. Forster C and Handwerker HO. Automatic classification and analysis of microneurographic spike data using a PC/AT. J Neurosci Methods 31: 109-118, 1990.
16. Ginouves A, Ilc K, Macias N, Pouyssegur J, and Berra E. PHDs overactivation during chronic hypoxia ''desensitizes'' HIFalpha and protects cells from necrosis. Proc Natl Acad Sci USA 105: 4745-4750, 2008.
17. Guhring H, Tegeder I, Lotsch J, Pahl A, Werner U, Reeh PW, Rehse K, Brune K, and Geisslinger G. Role of nitric oxide in zymosan induced paw inflammation and thermal hyper-algesia. Inflamm Res 50: 83-88, 2001.
18. Hawkes HJ, Karlenius TC, and Tonissen KF. Regulation of the human thioredoxin gene promoter and its key substrates: a study of functional and putative regulatory elements. Biochim Biophys Acta 1840: 303-314, 2013.
19. Jin XG, Chen SR, Cao XH, Li L, and Pan HL. Nitric oxide inhibits nociceptive transmission by differentially regulating glutamate and glycine release to spinal dorsal horn neurons. J Biol Chem 286: 33190-33202, 2011.
20. Kakizawa S, Yamazawa T, Chen Y, Ito A, Murayama T, Oyamada H, Kurebayashi N, Sato O, Watanabe M, Mori N, Oguchi K, Sakurai T, Takeshima H, Saito N, and Iino M. Nitric oxide-induced calcium release via ryanodine receptors regulates neuronal function. Embo J 31: 417-428, 2012.
21. Kallenborn-Gerhardt W, Lu R, Syhr KMJ, Heidler J, von Melchner H, Geisslinger G, Bangsow T, and Schmidtko A. Antioxidant Activity of Sestrin 2 Controls Neuropathic Pain After Peripheral Nerve Injury. Antioxid Redox Signal 19:2013-2023, 2013.
22. Kallenborn-Gerhardt W, Schroder K, Del Turco D, Lu R, Kynast K, Kosowski J, Niederberger E, Shah AM, Brandes RP, Geisslinger G, and Schmidtko A. NADPH oxidase-4 maintains neuropathic pain after peripheral nerve injury. J Neurosci 32: 10136-10145, 2012.
23. Kaneko S, Kawakami S, Hara Y, Wakamori M, Itoh E, Minami T, Takada Y, Kume T, Katsuki H, Mori Y, and Akaike A. A critical role of TRPM2 in neuronal cell death by hydrogen peroxide. J Pharmacol Sci 101: 66-76, 2006.
24. Kawasaki Y, Xu ZZ, Wang X, Park JY, Zhuang ZY, Tan PH, Gao YJ, Roy K, Corfas G, Lo EH, and Ji RR. Distinct roles of matrix metalloproteases in the early-and late-phase development of neuropathic pain. Nat Med 14: 331-336, 2008.
25. Keswani SC, Bosch-Marce M, Reed N, Fischer A, Semenza GL, and Hoke A. Nitric oxide prevents axonal degeneration by inducing HIF-1-dependent expression of erythropoietin. Proc Natl Acad Sci USA 108: 4986-4990, 2011.
26. Kim D, You B, Jo EK, Han SK, Simon MI, and Lee SJ. NADPH oxidase 2-derived reactive oxygen species in spinal cord microglia contribute to peripheral nerve injury-induced neuropathic pain. Proc Natl Acad Sci USA 107: 14851-14856, 2010.
27. Kim KS, Yoo HY, Park KS, Kim JK, Zhang YH, and Kim SJ. Differential effects of acute hypoxia on the activation of TRPV1 by capsaicin and acidic pH. J Physiol Sci 62: 93-103, 2012.
28. King RH, Chandler D, Lopaticki S, Huang D, Blake J, Muddle JR, Kilpatrick T, Nourallah M, Miyata T, Okuda T, Carter KW, Hunter M, Angelicheva D, Morahan G, and Kalaydjieva L. Ndrg1 in development and maintenance of the myelin sheath. Neurobiol Dis 42: 368-380, 2011.
29. Kobayashi H, Chattopadhyay S, Kato K, Dolkas J, Kikuchi S, Myers RR, and Shubayev VI. MMPs initiate Schwann cellmediated MBP degradation and mechanical nociception after nerve damage. Mol Cell Neurosci 39: 619-627, 2008.
30. Koshiji M and Huang LE. Dynamic balancing of the dual nature of HIF-1alpha for cell survival. Cell Cycle 3: 853-854, 2004.
31. Li F, Sonveaux P, Rabbani ZN, Liu S, Yan B, Huang Q, Vujaskovic Z, Dewhirst MW, and Li CY. Regulation of HIF-1alpha stability through S-nitrosylation. Mol Cell 26: 63-74, 2007.
32. Lu DY, Liou HC, Tang CH, and Fu WM. Hypoxia-induced iNOS expression in microglia is regulated by the PI3-kinase/Akt/mTOR signaling pathway and activation of hypoxia in-ducible factor-1alpha. Biochem Pharmacol 72: 992-1000, 2006.
33. Martin LJ, Adams NA, Pan Y, Price A, and Wong M. The mitochondrial permeability transition pore regulates nitric oxide-mediated apoptosis of neurons induced by target deprivation. J Neurosci 31: 359-370, 2011.
34. Meller ST, Lewis SJ, Bates JN, Brody MJ, and Gebhart GF. Is there a role for an endothelium-derived relaxing factor in nociception? Brain Res 531: 342-345, 1990.
35. Metzen E, Zhou J, Jelkmann W, Fandrey J, and Brune B. Nitric oxide impairs normoxic degradation of HIF-1alpha by inhibition of prolyl hydroxylases. Mol Biol Cell 14: 3470-3481, 2003.
36. Miyamoto T, Dubin AE, Petrus MJ, and Patapoutian A. TRPV1 and TRPA1 mediate peripheral nitric oxide-induced nociception in mice. PLoS One 4: e7596, 2009.
37. Ogunshola OO and Antoniou X. Contribution of hypoxia to Alzheimer's disease: is HIF-1alpha a mediator of neurode-generation? Cell Mol Life Sci 66: 3555-3563, 2009.
38. Okuda T, Higashi Y, Kokame K, Tanaka C, Kondoh H, and Miyata T. Ndrg1-deficient mice exhibit a progressive de-myelinating disorder of peripheral nerves. Mol Cell Biol 24: 3949-3956, 2004.
39. Olson N, Hristova M, Heintz NH, Lounsbury KM, and van der Vliet A. Activation of hypoxia-inducible factor-1 protects airway epithelium against oxidant-induced barrier dysfunction. Am J Physiol Lung Cell Mol Physiol 301: L993-L1002, 2011.
40. Petruska JC, Napaporn J, Johnson RD, Gu JG, and Cooper BY. Subclassified acutely dissociated cells of rat DRG: his-tochemistry and patterns of capsaicin-, proton-, and ATP-activated currents. J Neurophysiol 84: 2365-2379, 2000.
41. Pickert G, Myrczek T, Ruckert S, Weigert A, Haussler A, Ferreiros N, Brune B, Lotsch J, and Tegeder I. Inhibition of GTP cyclohydrolase reduces cancer pain in mice and enhances analgesic effects of morphine. J Mol Med (Berl) 90: 1473-1486, 2012.
42. Rice ME. H2O2: a dynamic neuromodulator. Neuroscientist 17: 389-406, 2011.
43. Rigaud M, Gemes G, Weyker PD, Cruikshank JM, Kawano T, Wu HE, and Hogan QH. Axotomy depletes intracellular calcium stores in primary sensory neurons. Anesthesiology 111: 381-392, 2009.
44. Ristoiu V, Shibasaki K, Uchida K, Zhou Y, Ton BH, Flonta ML, and Tominaga M. Hypoxia-induced sensitization of transient receptor potential vanilloid 1 involves activation of hypoxia-inducible factor-1 alpha and PKC. Pain 152: 936-945, 2011.
45. Sawada Y, Hosokawa H, Matsumura K, and Kobayashi S. Activation of transient receptor potential ankyrin 1 by hydrogen peroxide. Eur J Neurosci 27: 1131-1142, 2008.
46. Scheving R, Wittig I, Heide H, Albuquerque B, Steger M, Brandt U, and Tegeder I. Protein S-nitrosylation and deni-trosylation in the mouse spinal cord upon injury of the sciatic nerve. J Proteomics 75: 3987-4004, 2012.
47. Schmidtko A, Tegeder I, and Geisslinger G. No NO, no pain? The role of nitric oxide and cGMP in spinal pain processing. Trends Neurosci 32: 339-346, 2009.
48. Scholz J and Woolf CJ. The neuropathic pain triad: neurons, immune cells and glia. Nat Neurosci 10: 1361-1368, 2007.
49. Semenza GL. Hypoxia-inducible factor 1: oxygen homeostasis and disease pathophysiology. Trends Mol Med 7: 345-350, 2001.
50. Sharp FR and Bernaudin M. HIF1 and oxygen sensing in the brain. Nat Rev Neurosci 5: 437-448, 2004.
51. Takahashi N, Kozai D, Kobayashi R, Ebert M, and Mori Y. Roles of TRPM2 in oxidative stress. Cell Calcium 50: 279-287, 2011.
52. Takahashi N, Kuwaki T, Kiyonaka S, Numata T, Kozai D, Mizuno Y, Yamamoto S, Naito S, Knevels E, Carmeliet P, Oga T, Kaneko S, Suga S, Nokami T, Yoshida J, and Mori Y. TRPA1 underlies a sensing mechanism for O2. Nat Chem Biol 7: 701-711, 2011.
53. Tandrup T, Woolf CJ, and Coggeshall RE. Delayed loss of small dorsal root ganglion cells after transection of the rat sciatic nerve. J Comp Neurol 422: 172-180, 2000.
54. Tegeder I, Costigan M, Griffin RS, Abele A, Belfer I, Schmidt H, Ehnert C, Nejim J, Marian C, Scholz J, Wu T, Allchorne A, Diatchenko L, Binshtok AM, Goldman D, Adolph J, Sama S, Atlas SJ, Carlezon WA, Parsegian A, Lotsch J, Fillingim RB, Maixner W, Geisslinger G, Max MB, and Woolf CJ. GTP cyclohydrolase and tetrahydrobio-pterin regulate pain sensitivity and persistence. Nat Med 12: 1269-1277, 2006.
55. Tegeder I, Scheving R, Wittig I, and Geisslinger G. SNO-ing at the Nociceptive Synapse? Pharmacol Rev 63: 366-389, 2011.
56. Ueno S, Tsuda M, Iwanaga T, and Inoue K. Cell type-specific ATP-activated responses in rat dorsal root ganglion neurons. Br J Pharmacol 126: 429-436, 1999.
57. Werno C, Menrad H, Weigert A, Dehne N, Goerdt S, Schledzewski K, Kzhyshkowska J, and Brune B. Knockout of HIF-1alpha in tumor-associated macrophages enhances M2 polarization and attenuates their pro-angiogenic responses. Carcinogenesis 31: 1863-1872, 2010.
58. Yoshida T, Inoue R, Morii T, Takahashi N, Yamamoto S, Hara Y, Tominaga M, Shimizu S, Sato Y, and Mori Y. Nitric oxide activates TRP channels by cysteine S-nitrosylation. Nat Chem Biol 2: 596-607, 2006.
59. Yu X, Fang Y, Liu H, Zhu J, Zou J, Xu X, Jiang S, and Ding X. The balance of beneficial and deleterious effects of hypoxia-inducible factor activation by prolyl hydroxylase inhibitor in rat remnant kidney depends on the timing of administration. Nephrol Dial Transplant 27: 3110-3119, 2012.
60. Yuan G, Khan SA, Luo W, Nanduri J, Semenza GL, and Prabhakar NR. Hypoxia-inducible factor 1 mediates increased expression of NADPH oxidase-2 in response to intermittent hypoxia. J Cell Physiol 226: 2925-2933, 2011.
61. Zhou J and Brune B. NO and transcriptional regulation: from signaling to death. Toxicology 208: 223-233, 2005.
62. Zimmermann K, Lennerz JK, Hein A, Link AS, Kaczmarek JS, Delling M, Uysal S, Pfeifer JD, Riccio A, and Clapham DE. Transient receptor potential cation channel, subfamily C, member 5 (TRPC5) is a cold-transducer in the peripheral nervous system. Proc Natl Acad Sci USA 108: 18114-18119, 2011.