Participation of transient receptor potential vanilloid 1 in paclitaxel-induced acute visceral and peripheral nociception in rodents.

Published on Jun 5, 2018in European Journal of Pharmacology3.263
· DOI :10.1016/J.EJPHAR.2018.03.033
Mateus Rossato16
Estimated H-index: 16
(USP: University of São Paulo),
Flávia Karine Rigo17
Estimated H-index: 17
(Health Science University)
+ 6 AuthorsGabriela Trevisan25
Estimated H-index: 25
(UFSM: Universidade Federal de Santa Maria)
Abstract The clinical use of paclitaxel as a chemotherapeutic agent is limited by the severe acute and chronic hypersensitivity caused when it is administered via intraperitoneal or intravenous routes. Thus far, evidence has suggested that transient receptor potential vanilloid-1 (TRPV1) has a key role in the chronic neuropathy induced by paclitaxel. Despite this, the role of TRPV1 in paclitaxel -related acute nociception, especially the development of visceral nociception, has not been evaluated. Thus, the goal of this study was to evaluate the participation of TRPV1 in a model of acute nociception induced by paclitaxel in rats and mice. A single intraperitoneal (i.p.) paclitaxel administration (1 mg/kg, i.p.) produced an immediate visceral nociception response 1 h after administration, caused mechanical and heat hypersensitivity, and diminished burrowing behaviour 24 h after administration. These nociceptive responses were reduced by SB-366791 treatment (0.5 mg/kg, i.p., a TRPV1 antagonist). In addition, TRPV1-positive sensory fibre ablation (using resiniferatoxin, 200 µg/kg, s.c.) reduced visceral nociception and mechanical or heat hypersensitivity caused by paclitaxel injection. Similarly, TRPV1 deficient mice showed a pronounced reduction in mechanical allodynia to paclitaxel acute injection and did not develop heat hypersensitivity. Moreover, 24 h after its injection, paclitaxel induced chemical hypersensitivity to capsaicin (a TRPV1 agonist, 0.01 nmol/site) and increased TRPV1 immunoreactivity in the dorsal root ganglion and sciatic nerve. In conclusion, TRPV1 is involved in mechanical and heat hypersensitivity and spontaneous-pain behaviour induced 24 h after a single paclitaxel injection. This receptor is also involved in visceral nociception induced immediately after paclitaxel administration.
📖 Papers frequently viewed together
9 Authors (Tomomi Hara, ..., Kyoji Taguchi)
81 Citations
24 Citations
4 Citations
#1Mingyue Zhang (HMU: Harbin Medical University)H-Index: 3
#2Meng Chi (HMU: Harbin Medical University)H-Index: 2
Last. Guonian Wang (HMU: Harbin Medical University)H-Index: 5
view all 6 authors...
Morphine is widely used as an analgesic to treat moderate to severe pain, but chronic morphine use is associated with development of tolerance and dependence, which limits its analgesic efficacy. Our previous research has showed that nonanalgetic dose of a cannabinoid type 2 (CB2) receptor agonist reduced morphine tolerance in cancer pain. A previous study showed the colocalization of CB2 and transient receptor potential vanilloid 1 (TRPV1) in human and rat dorsal root ganglia (DRG) sensory neur...
6 CitationsSource
#1Jennifer R. Deuis (UQ: University of Queensland)H-Index: 19
#2Lucie S. Dvorakova (UQ: University of Queensland)H-Index: 4
Last. Irina Vetter (UQ: University of Queensland)H-Index: 37
view all 3 authors...
Rodents are commonly used to study the pathophysiological mechanisms of pain as studies in humans may be difficult to perform and ethically limited. As pain cannot be directly measured in rodents, many methods that quantify "pain-like" behaviors or nociception have been developed. These behavioral methods can be divided into stimulus-evoked or non-stimulus evoked (spontaneous) nociception, based on whether or not application of an external stimulus is used to elicit a withdrawal response. Stimul...
263 CitationsSource
#1M. V. Storozhuk (NAS: National Academy of Sciences)H-Index: 10
#2Alexander Zholos (NAS: National Academy of Sciences)H-Index: 30
BACKGROUND:Chronic pain is a significant clinical problem and a very complex pathophysiological phenomenon. There is growing evidence that targeting the endocannabinoid system may be a useful approach to pain alleviation. Classically, the system includes G protein-coupled receptors of the CB1 and CB2 subtypes and their endogenous ligands. More recently, several subtypes of the large superfamily of cation TRP channels have been coined as "ionotropic cannabinoid receptors", thus highlighting their...
34 CitationsSource
#1Yili WuH-Index: 21
#2Xin WangH-Index: 7
Last. Bo Bai (Jining Medical University)H-Index: 4
view all 6 authors...
Stroke is one of the leading causes of death and disability worldwide, and ischemic stroke accounts for approximately 87% of cases. Improving post-stroke recovery is a major challenge in stroke treatment. Accumulated evidence indicates that the apelinergic system, consisting of apelin and apelin receptor, is temporally dysregulated in ischemic stroke. Moreover, the apelinergic system plays a pivotal role in post-stroke recovery by inhibiting neuronal apoptosis and facilitating angiogenesis throu...
210 CitationsSource
#1Marco Sisignano (Goethe University Frankfurt)H-Index: 16
#2Carlo Angioni (Goethe University Frankfurt)H-Index: 27
Last. Gerd Geisslinger (Goethe University Frankfurt)H-Index: 90
view all 24 authors...
Chemotherapy-induced peripheral neuropathic pain (CIPNP) is a severe dose- and therapy-limiting side effect of widely used cytostatics that is particularly difficult to treat. Here, we report increased expression of the cytochrome-P450-epoxygenase CYP2J6 and increased concentrations of its linoleic acid metabolite 9,10-EpOME (9,10-epoxy-12Z-octadecenoic acid) in dorsal root ganglia (DRGs) of paclitaxel-treated mice as a model of CIPNP. The lipid sensitizes TRPV1 ion channels in primary sensory n...
45 CitationsSource
#1Yan LiH-Index: 19
#2Pavel AdamekH-Index: 5
Last. Patrick M. DoughertyH-Index: 75
view all 19 authors...
Peripheral neuropathy is dose limiting in paclitaxel cancer chemotherapy and can result in both acute pain during treatment and chronic persistent pain in cancer survivors. The hypothesis tested was that paclitaxel produces these adverse effects at least in part by sensitizing transient receptor potential vanilloid subtype 1 (TRPV1) through Toll-like receptor 4 (TLR4) signaling. The data show that paclitaxel-induced behavioral hypersensitivity is prevented and reversed by spinal administration o...
125 CitationsSource
#1Xisheng Yan (UGA: University of Georgia)H-Index: 11
#2Dylan W. Maixner (UGA: University of Georgia)H-Index: 7
Last. Han-Rong Weng (UGA: University of Georgia)H-Index: 32
view all 7 authors...
Paclitaxel, a powerful anti-neoplastic drug, often causes pathological pain, which significantly reduces the quality of life in patients. Paclitaxel-induced pain includes pain that occurs immediately after paclitaxel treatment (paclitaxel-associated acute pain syndrome, P-APS) and pain that persists for weeks to years after cessation of paclitaxel treatment (paclitaxel induced chronic neuropathic pain). Mechanisms underlying P-APS remain unknown. In this study, we found that paclitaxel causes ac...
28 CitationsSource
#1Manouela V. Valtcheva (WashU: Washington University in St. Louis)H-Index: 8
#2Steve Davidson (WashU: Washington University in St. Louis)H-Index: 18
Last. Robert W. Gereau (WashU: Washington University in St. Louis)H-Index: 63
view all 5 authors...
Background: Itch-producing compounds stimulate receptors expressed on small diameter fibers that innervate the skin. Many of the currently known pruritogen receptors are Gq Protein-Coupled Receptors (GqPCR), which activate Protein Kinase C (PKC). Specific isoforms of PKC have been previously shown to perform selective functions; however, the roles of PKC isoforms in regulating itch remain unclear. In this study, we investigated the novel PKC isoform PKCδ as an intracellular modulator of itch sig...
41 CitationsSource
Oxaliplatin, a commonly used chemotherapeutic agent, is associated with both acute and chronic neurotoxicity. Chronic sensory neuropathy can be dose limiting and may have detrimental effects on patients’ quality of life. Preclinical studies provide an understanding of the pathophysiology of chemotherapy-induced peripheral neuropathy (CIPN) and may be important for developing effective preventative interventions. In this issue of the JCI, Coriat and colleagues used an animal model and a human pil...
17 CitationsSource
#1Flávia Karine Rigo (UFMG: Universidade Federal de Minas Gerais)H-Index: 17
#2Gerusa Duarte Dalmolin (UFSM: Universidade Federal de Santa Maria)H-Index: 15
Last. Marcus Vinicius Gomez (UFMG: Universidade Federal de Minas Gerais)H-Index: 35
view all 12 authors...
Abstract The treatment with the chemotherapeutic agent paclitaxel produces a painful peripheral neuropathy, and is associated with an acute pain syndrome in a clinically significant number of patients. However, no standard therapy has been established to manage the acute pain or the chronic neuropathic pain related to paclitaxel. In the present study, we evaluated the analgesic potential of two N-type voltage-gated calcium channel (VGCC) blockers, ω-conotoxin MVIIA and Phα1β, on acute and chroni...
48 CitationsSource
Cited By12
#1Cornelia J C Vermeer (UU: Utrecht University)
#2Anouk E. Hiensch (UU: Utrecht University)H-Index: 2
Last. Niels Eijkelkamp (UU: Utrecht University)H-Index: 23
view all 5 authors...
Background null Paclitaxel is a taxane-based chemotherapeutic agent used as a treatment in breast cancer. There is no effective prevention or treatment strategy for the most common side effect of peripheral neuropathy. In this manuscript, we reviewed the molecular mechanisms that contribute to paclitaxel-induced peripheral neuropathy (PIPN) with an emphasis on immune-related processes. null Methods null A systematic search of the literature was conducted in PubMed, EMBASE and Cochrane Library. T...
#1Yi Han Liao (NCKU: National Cheng Kung University)H-Index: 3
#2Yi-Chi Su (NCKU: National Cheng Kung University)
Last. Lung Yu (NCKU: National Cheng Kung University)H-Index: 28
view all 9 authors...
Rationale and objective null This study was undertaken to assess the modulating effects of (1) pre-exposure to repeated social disruption and (2) group testing on writhing associated with visceral pain induced by intraperitoneal administration of acetic acid. null Materials and methods null Six consecutive days of social disruption were used to prime for stress, while group testing referred to 3 mouse cage-mates receiving the acetic acid-induced writhing test as a group. null Results null Social...
#1Shi-Yu Deng (Guangzhou Medical University)H-Index: 1
#2Xuechun Tang (Shihezi University)
Last. Jun-Qiang Si (Shihezi University)H-Index: 12
view all 11 authors...
Our aim was to investigate the effects of the protein expression and the function of sodium, potassium and chloride co-transporter (NKCC1) in the dorsal root ganglion (DRG) after activation of transient receptor potential vanilloid 1 receptor (TRPV1) in capsaicin-induced acute neurogenic inflammatory pain and the possible mechanism of action. Male Sprague Dawley rats were randomly divided into control , capsaicin and inhibitor groups. The expression and distribution of TRPV1 and NKCC1 in rat DRG...
#1Gary R. Lewin (MDC: Max Delbrück Center for Molecular Medicine)H-Index: 71
#2Ewan St. John Smith (University of Cambridge)H-Index: 24
Last. Thomas J. Park (UIC: University of Illinois at Chicago)H-Index: 33
view all 0 authors...
The naked mole-rat (Heterocephalus glaber) is famous for its longevity and unusual physiology. This eusocial species that lives in highly ordered and hierarchical colonies with a single breeding queen, also discovered secrets enabling somewhat pain-free living around 20 million years ago. Unlike most mammals, naked mole-rats do not feel the burn of chili pepper's active ingredient, capsaicin, nor the sting of acid. Indeed, by accumulating mutations in genes encoding proteins that are only now be...
1 CitationsSource
#1Jiali Wang (SZU: Shenzhen University)H-Index: 2
#2Changyu Jiang (SZU: Shenzhen University)H-Index: 14
Last. Yue Hao (SZU: Shenzhen University)H-Index: 5
view all 8 authors...
Rationale Paclitaxel-induced acute pain syndrome (P-APS), characterized by deep muscle aches and arthralgia, occurs in more than 70% of patients who receive paclitaxel. P-APS can be debilitating for patients and lead to reductions and discontinuation of potentially curable therapy. Despite being relatively common in clinical practice, no clear treatment exists for P-APS and the underlying mechanisms remain poorly defined. Regulation of glutamatergic transmission by metabotropic glutamate recepto...
2 CitationsSource
#1Indiara Brusco (UFSM: Universidade Federal de Santa Maria)H-Index: 10
#2Simone Li Puma (UniFI: University of Florence)H-Index: 8
Last. Gabriela Trevisan (UFSM: Universidade Federal de Santa Maria)H-Index: 25
view all 15 authors...
: Antineoplastic therapy has been associated with pain syndrome development characterized by acute and chronic pain. The chemotherapeutic agent dacarbazine, used mainly to treat metastatic melanoma, is reported to cause painful symptoms, compromising patient quality of life. Evidence has proposed that transient receptor potential ankyrin 1 (TRPA1) plays a critical role in chemotherapy-induced pain syndrome. Here, we investigated whether dacarbazine causes painful hypersensitivity in naive or mel...
8 CitationsSource
#1Susana Paula Moreira Fischer (UFSM: Universidade Federal de Santa Maria)H-Index: 3
#2Indiara Brusco (UFSM: Universidade Federal de Santa Maria)H-Index: 10
Last. Sara Marchesan Oliveira (UFSM: Universidade Federal de Santa Maria)H-Index: 25
view all 9 authors...
Abstract Fibromyalgia is characterised mainly by symptoms of chronic widespread pain and comorbidities like depression. Although these symptoms cause a notable impact on the patient's quality of life, the underlying aetiology and pathophysiology of this disease remain incompletely elucidated. The transient receptor potential vanilloid type 1 (TRPV1) is a polymodal receptor that is involved in the development of nociceptive and depressive behaviours, while α-spinasterol, a multitarget TRPV1 antag...
5 CitationsSource
#1Yuanyuan Li (ZJNU: Zhejiang Chinese Medical University)H-Index: 5
#2Chengyu Yin (ZJNU: Zhejiang Chinese Medical University)H-Index: 6
Last. Boyi LiuH-Index: 17
view all 11 authors...
Paclitaxel-induced peripheral neuropathy is a common adverse effect during paclitaxel treatment resulting in sensory abnormalities and neuropathic pain during chemotherapy and in cancer survivors. Conventional therapies are usually ineffective and possess adverse effects. Here, we examined the effects of electroacupuncture (EA) on a rat model of paclitaxel-induced neuropathic pain and related mechanisms. EA robustly and persistently alleviated paclitaxel-induced pain hypersensitivities. Mechanis...
24 CitationsSource
#1Kenny Roman (NU: Northwestern University)H-Index: 6
#2Christel Hall (NU: Northwestern University)H-Index: 3
Last. Praveen Thumbikat (NU: Northwestern University)H-Index: 21
view all 4 authors...
BACKGROUND: Chronic prostatitis/chronic pelvic pain syndrome (CP/CPPS) is a disorder that is characterized by persistent pelvic pain in men of any age. Although several studies suggest that the transient receptor potential vanilloid 1 (TRPV1) channel is involved in various pathways of chronic pain, the TRPV1 channel has not been implicated in chronic pelvic pain associated with CP/CPPS. METHODS: Male C57BL/6J (B6) and TRPV1 knockout (TRPV1 KO) mice (5-7 weeks old) were used to study the developm...
4 CitationsSource
#1Lin LiH-Index: 3
#2Jinxiu Li (UTMB: University of Texas Medical Branch)H-Index: 1
Last. Qing YangH-Index: 11
view all 6 authors...
Abstract Paclitaxel-induced peripheral neuropathy (PIPN) and associated neuropathic pain are the most common and serious adverse effects experienced by cancer patients receiving paclitaxel treatment. These effects adversely impact daily activities and consequently the quality of life, sometimes forcing the suspension of treatment and negatively influencing survival. Patients are usually at high risk of developing PIPN if paclitaxel induces acute pain, which strongly suggests that an acute increa...
9 CitationsSource