Novel therapeutic strategy to prevent chemotherapy-induced persistent sensory neuropathy by TRPA1 blockade

Cancer Research

Volumn 73, Issue 10, 2013, Pages 3120-3131

  Trevisan, Gabriela ^a,b   Materazzi, Serena ^b   Fusi, Camilla ^b   Altomare, Alessandra ^c   Aldini, Giancarlo ^c   Lodovici, Maura ^b   Patacchini, Riccardo ^d   Geppetti, Pierangelo ^b   Nassini, Romina ^b  

^a FEDERAL UNIVERSITY OF SANTA MARIA   (Brazil)

^b UNIVERSITY OF FLORENCE   (Italy)

^c UNIVERSITY OF MILAN   (Italy)

^d CHIESI FARMACEUTICI S P A   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

6 N CARBOXYMETHYLLYSINE; ALLYL ISOTHIOCYANATE; BORTEZOMIB; N (4 ISOPROPYLPHENYL) 2 (1,2,3,6 TETRAHYDRO 1,3 DIMETHYL 2,6 DIOXO 7H PURIN 7 YL)ACETAMIDE; OXALIPLATIN; THIOCTIC ACID; TRANSIENT RECEPTOR POTENTIAL CHANNEL A1;

AMINO ACID BLOOD LEVEL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHEMOTHERAPY INDUCED PERSISTENT SENSORY NEUROPATHY; CONTROLLED STUDY; DRUG EFFECT; DRUG SAFETY; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SENSORY NEUROPATHY; SYSTEMIC THERAPY; TREATMENT DURATION;

ACETANILIDES; ANIMALS; ANTINEOPLASTIC AGENTS; BORONIC ACIDS; MICE; MICE, INBRED C57BL; ORGANOPLATINUM COMPOUNDS; PERIPHERAL NERVOUS SYSTEM DISEASES; PURINES; PYRAZINES; THIOCTIC ACID; TRANSIENT RECEPTOR POTENTIAL CHANNELS;

EID: 84877844157     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-12-4370     Document Type: Article

References (48)

1. Cavaletti G, Marmiroli P. Chemotherapy-induced peripheral neurotoxicity. Nat Rev Neurol 2010;6:657-66.
2. Alessandri-Haber N, Dina OA, Joseph EK, Reichling DB, Levine JD. Interaction of transient receptor potential vanilloid 4, integrin, and SRC tyrosine kinase in mechanical hyperalgesia. J Neurosci 2008;28: 1046-57. (Pubitemid 351186354)
3. Joseph EK, Chen X, Bogen O, Levine JD. Oxaliplatin acts on IB4-positive nociceptors to induce an oxidative stress-dependent acute painful peripheral neuropathy. J Pain 2008;9:463-72.
4. Gauchan P, Andoh T, Kato A, Sasaki A, Kuraishi Y. Effects of the prostaglandin E1 analog limaprost on mechanical allodynia caused by chemotherapeutic agents in mice. J Pharmacol Sci 2009;109:469-72.
5. Descoeur J, Pereira V, Pizzoccaro A, Francois A, Ling B, Maffre V, et al. Oxaliplatin-induced cold hypersensitivity is due to remodelling of ion channel expression in nociceptors. EMBO Mol Med 2011;3:266-78.
6. Nassini R, Gees M, Harrison S, De Siena G, Materazzi S, Moretto N, et al. Oxaliplatin elicits mechanical and cold allodynia in rodents via TRPA1 receptor stimulation. Pain 2011;152:1621-31.
7. Xiao WH, Bennett GJ. Effects of mitochondrial poisons on the neuropathic pain produced by the chemotherapeutic agents, paclitaxel and oxaliplatin. Pain 2012;153:704-9.
8. Pachman DR, Barton DL, Watson JC, Loprinzi CL. Chemotherapyinduced peripheral neuropathy: Prevention and treatment. Clin Pharmacol Ther 2011;90:377-87.
9. Barriere DA, Rieusset J, Chanteranne D, Busserolles J, Chauvin MA, Chapuis L, et al. Paclitaxel therapy potentiates cold hyperalgesia in streptozotocin-induced diabetic rats through enhanced mitochondrial reactive oxygen species production and TRPA1 sensitization. Pain 2012;153:553-61.
10. Jaggi AS, Singh N. Mechanisms in cancer-chemotherapeutic drugsinduced peripheral neuropathy. Toxicology 2012;291:1-9.
11. Story GM, Peier AM, Reeve AJ, Eid SR, Mosbacher J, Hricik TR, et al. ANKTM1, a TRP-like channel expressed in nociceptive neurons, is activated by cold temperatures. Cell 2003;112:819-29. (Pubitemid 36378884)
12. Nilius B, Owsianik G, Voets T, Peters JA. Transient receptor potential cation channels in disease. Physiol Rev 2007;87:165-217. (Pubitemid 46207713)
13. Trevisani M, Siemens J, Materazzi S, Bautista DM, Nassini R, Campi B, et al. 4-Hydroxynonenal, an endogenous aldehyde, causes pain and neurogenic inflammation through activation of the irritant receptor TRPA1. Proc Natl Acad Sci U S A 2007;104:13519-24. (Pubitemid 47293977)
14. Andersson DA, Gentry C, Moss S, Bevan S. Transient receptor potential A1 is a sensory receptor for multiple products of oxidative stress. J Neurosci 2008;28:2485-94. (Pubitemid 351348185)
15. Materazzi S, Nassini R, Andre E, Campi B, Amadesi S, Trevisani M, et al. Cox-dependent fatty acid metabolites cause pain through activation of the irritant receptor TRPA1. Proc Natl Acad Sci U S A 2008;105:12045-50.
16. Sawada Y, Hosokawa H, Matsumura K, Kobayashi S. Activation of transient receptor potential ankyrin 1 by hydrogen peroxide. Eur J Neurosci 2008;27:1131-42. (Pubitemid 351432345)
17. Paramore A, Frantz S. Bortezomib. Nat Rev Drug Discov 2003;2: 611-2.
18. Cata JP, Weng HR, Burton AW, Villareal H, Giralt S, Dougherty PM. Quantitative sensory findings in patients with bortezomib-induced pain. J Pain 2007;8:296-306. (Pubitemid 46551871)
19. Mohty B, El-Cheikh J, Yakoub-Agha I, Moreau P, Harousseau JL, Mohty M. Peripheral neuropathy and new treatments for multiple myeloma: Background and practical recommendations. Haematologica 2010;95:311-9.
20. Broyl A, Corthals SL, Jongen JL, van der Holt B, Kuiper R, de Knegt Y, et al. Mechanisms of peripheral neuropathy associated with bortezomib and vincristine in patients with newly diagnosed multiple myeloma: A prospective analysis of data from the HOVON-65/GMMG-HD4 trial. Lancet Oncol 2010;11:1057-65.
21. Premkumar DR, Jane EP, Agostino NR, Didomenico JD, Pollack IF. Bortezomib-induced sensitization of malignant human glioma cells to vorinostat-induced apoptosis depends on reactive oxygen species production, mitochondrial dysfunction, Noxa upregulation, Mcl-1 cleavage, and DNA damage. Mol Carcinog 2011;2011:21835.
22. Shin YK, Jang SY, Lee HK, Jung J, Suh DJ, Seo SY, et al. Pathological adaptive responses of Schwann cells to endoplasmic reticulum stress in bortezomib-induced peripheral neuropathy. Glia 2010;58:1961-76.
23. Nakano A, Abe M,Oda A,AmouH, Hiasa M, Nakamura S, et al. Delayed treatment with vitamin C and N-acetyl-L-cysteine protects Schwann cells without compromising the anti-myeloma activity of bortezomib. Int J Hematol 2011;93:727-35.
24. Zhao M, Isami K, Nakamura S, Shirakawa H, Nakagawa T, Kaneko S. Acute cold hypersensitivity characteristically induced by oxaliplatin is caused by the enhanced responsiveness of TRPA1 in mice. Mol Pain 2012;8:55.
25. Cavaletti G, Gilardini A, Canta A, Rigamonti L, Rodriguez-Menendez V, Ceresa C, et al. Bortezomib-induced peripheral neurotoxicity: A neurophysiological and pathological study in the rat. Exp Neurol 2007;204:317-25. (Pubitemid 46330280)
26. Meregalli C, Canta A, Carozzi VA, Chiorazzi A, Oggioni N, Gilardini A, et al. Bortezomib-induced painful neuropathy in rats: A behavioral, neurophysiological and pathological study in rats. Eur J Pain 2009;14: 343-50.
27. Bruna J, Udina E, Ale A, Vilches JJ, Vynckier A, Monbaliu J, et al. Neurophysiological, histological and immunohistochemical characterization of bortezomib-induced neuropathy in mice. Exp Neurol 2010;223:599-608.
28. Carozzi VA, Canta A, Oggioni N, Sala B, Chiorazzi A, Meregalli C, et al. Neurophysiological and neuropathological characterization of new murine models of chemotherapy-induced chronic peripheral neuropathies. Exp Neurol 2010;226:301-9.
29. Materazzi S, Fusi C, Benemei S, Pedretti P, Patacchini R, Nilius B, et al. TRPA1 and TRPV4 mediate paclitaxel-induced peripheral neuropathy in mice via a glutathione-sensitive mechanism. Pflugers Arch 2012; 463:561-9.
30. Chaplan SR, Bach FW, Pogrel JW, Chung JM, Yaksh TL. Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Methods 1994;53:55-63. (Pubitemid 24238751)
31. Dixon WJ. Efficient analysis of experimental observations. Annu Rev Pharmacol Toxicol 1980;20:441-62.
32. Ferreira J, Campos MM, Araujo R, Bader M, Pesquero JB, Calixto JB. The use of kinin B1 and B2 receptor knockout mice and selective antagonists to characterize the nociceptive responses caused by kinins at the spinal level. Neuropharmacology 2002;43:1188-97. (Pubitemid 36013455)
33. Alessandri-Haber N, Joseph E, Dina OA, Liedtke W, Levine JD. TRPV4 mediates pain-related behavior induced by mild hypertonic stimuli in the presence of inflammatory mediator. Pain 2005;118:70-9. (Pubitemid 41566587)
34. Kassuya CA, Ferreira J, Claudino RF, Calixto JB. Intraplantar PGE2 causes nociceptive behaviour and mechanical allodynia: The role of prostanoid E receptors and protein kinases. Br J Pharmacol 2007;150: 727-37. (Pubitemid 46440219)
35. Trevisan G, Rossato MF, Walker CI, Klafke JZ, Rosa F, Oliveira SM, et al. Identification of the plant steroid alpha-spinasterol as a novel transient receptor potential vanilloid 1 antagonist with antinociceptive properties. J Pharmacol Exp Ther 2012;343:258-69.
36. da Costa DS, Meotti FC, Andrade EL, Leal PC, Motta EM, Calixto JB. The involvement of the transient receptor potential A1 (TRPA1) in the maintenance of mechanical and cold hyperalgesia in persistent inflammation. Pain 2009;148:431-7.
37. McNamara CR, Mandel-Brehm J, Bautista DM, Siemens J, Deranian KL, Zhao M, et al. TRPA1 mediates formalin-induced pain. Proc Natl Acad Sci U S A 2007;104:13525-30. (Pubitemid 47293978)
38. Alessandri-Haber N, Dina OA, Yeh JJ, Parada CA, Reichling DB, Levine JD. Transient receptor potential vanilloid 4 is essential in chemotherapy-induced neuropathic pain in the rat. J Neurosci 2004;24:4444-52. (Pubitemid 38608155)
39. Everaerts W, Zhen X, Ghosh D, Vriens J, Gevaert T, Gilbert JP, et al. Inhibition of the cation channel TRPV4 improves bladder function in mice and rats with cyclophosphamide-induced cystitis. Proc Natl Acad Sci U S A 2010;107:19084-9.
40. ObataK,KatsuraH,Mizushima T,YamanakaH,KobayashiK,Dai Y, et al. TRPA1 induced in sensory neurons contributes to cold hyperalgesia after inflammation and nerve injury. J Clin Invest 2005;115:2393-401. (Pubitemid 41266201)
41. Landowski TH, Megli CJ, Nullmeyer KD, Lynch RM, Dorr RT. Mitochondrial-mediated disregulation of Ca2+ is a critical determinant of Velcade (PS-341/bortezomib) cytotoxicity in myeloma cell lines. Cancer Res 2005;65:3828-36. (Pubitemid 40616363)
42. Wang HT, Liu ZG, Yang W, Liao AJ, Zhang R, Wu B, et al. [Study on mechanism of bortezomib inducing peripheral neuropathy and the reversing effect of reduced glutathione]. Zhonghua Xue Ye Xue Za Zhi 2011;32:107-11.
43. Aldini G, Dalle-Donne I, Facino RM, Milzani A, Carini M. Intervention strategies to inhibit protein carbonylation by lipoxidation-derived reactive carbonyls. Med Res Rev 2007;27:817-68. (Pubitemid 350035121)
44. Muthuraman A, Jaggi AS, Singh N, Singh D. Ameliorative effects of amiloride and pralidoxime in chronic constriction injury and vincristine induced painful neuropathy in rats. Eur J Pharmacol 2008; 587:104-11.
45. Bessac BF, Sivula M, von Hehn CA, Escalera J, Cohn L, Jordt SE. TRPA1 is a major oxidant sensor in murine airway sensory neurons. J Clin Invest 2008;118:1899-910. (Pubitemid 351632392)
46. Taylor-Clark TE, Ghatta S, Bettner W, Undem BJ. Nitrooleic acid, an endogenous product of nitrative stress, activates nociceptive sensory nerves via the direct activation of TRPA1. Mol Pharmacol 2009;75: 820-29.
47. Eid SR, Crown ED, Moore EL, Liang HA, Choong KC, Dima S, et al.HC-030031, a TRPA1 selective antagonist, attenuates inflammatory-and neuropathy-induced mechanical hypersensitivity. Mol Pain 2008;4: 48-58.
48. Morgado C, Pereira-Terra P, Tavares I. alpha-Lipoic acid normalizes nociceptive neuronal activity at the spinal cord of diabetic rats. Diabetes Obes Metab 2011;13:736-41.