Spontaneous and Bite-Evoked Muscle Pain Are Mediated by a Common Nociceptive Pathway With Differential Contribution by TRPV1

被引:35
作者
Wang, Sheng [1 ]
Lim, Jongseuk [1 ]
Joseph, John [1 ]
Wang, Sen [1 ]
Wei, Feng [1 ]
Ro, Jin Y. [1 ]
Chung, Man-Kyo [1 ]
机构
[1] Univ Maryland, Sch Dent, Ctr Adv Chron Pain Res, Dept Neural & Pain Sci,Program Neurosci, Baltimore, MD 21201 USA
基金
美国国家卫生研究院;
关键词
Muscle pain; nociceptors; inflammation; transient receptor potential vanilloid 1; dorsal horn; vanilloids; orofacial pain; DORSAL-HORN; GLUTAMATE RECEPTORS; TRIGEMINAL GANGLION; PRIMARY AFFERENTS; SPINAL NEURONS; SUBSTANCE-P; RAT; HYPERSENSITIVITY; HYPERALGESIA; MOUSE;
D O I
10.1016/j.jpain.2017.06.005
中图分类号
R74 [神经病学与精神病学];
学科分类号
摘要
Spontaneous pain and function-associated pain are prevalent symptoms of multiple acute and chronic muscle pathologies. We established mouse models for evaluating spontaneous pain and bite-evoked pain from masseter muscle, and determined the roles of transient receptor potential cation channel subfamily V member 1 (TRPV1) and the contribution of TRPV1- or neurokinin 1 (NK1)-dependent nociceptive pathways. Masseter muscle inflammation increased Mouse Grimace Scale scores and face-wiping behavior, which were attenuated by pharmacological or genetic inhibition of TRPV1. Masseter inflammation led to a significant reduction in bite force. Inhibition of TRPV1 only marginally relieved the inflammation-induced reduction of bite force. These results suggest a differential extent of contribution of TRPV1 to the 2 types of muscle pain. However, chemical ablation of TRPV1-expressing nociceptors or chemogenetic silencing of TRPV1-lineage nerve terminals in masseter muscle attenuated inflammation-induced changes in Mouse Grimace Scale scores as well as bite force. Furthermore, ablation of neurons expressing NK1 receptor in trigeminal subnucleus caudalis also prevented both types of muscle pain. Our results suggest that TRPV1 differentially contributes to spontaneous pain and bite-evoked muscle pain, but TRPV1-expressing afferents and NK1-expressing second order neurons commonly mediate both types of muscle pain. Therefore, manipulation of the nociceptive circuit may provide a novel approach for management of acute or chronic craniofacial muscle pain. Perspective: We report the profound contribution of TRPV1 to spontaneous muscle pain but not to bite-evoked muscle pain. These 2 types of muscle pain are transmitted through a common nociceptive pathway. These results may help to develop new strategies to manage multiple modes of muscle pain simultaneously by manipulating pain circuits. (C) 2017 by the American Pain Society
引用
收藏
页码:1333 / 1345
页数:13
相关论文
共 61 条
[1]   Role for monocyte chemoattractant protein-1 in the induction of chronic muscle pain in the rat [J].
Alvarez, Pedro ;
Green, Paul G. ;
Levine, Jon D. .
PAIN, 2014, 155 (06) :1161-1167
[2]   IB4-saporin attenuates acute and eliminates chronic muscle pain in the rat [J].
Alvarez, Pedro ;
Gear, Robert W. ;
Green, Paul G. ;
Levine, Jon D. .
EXPERIMENTAL NEUROLOGY, 2012, 233 (02) :859-865
[3]   Chemical phenotypes of muscle and cutaneous afferent neurons in the rat trigeminal ganglion [J].
Ambalavanar, R ;
Moritani, M ;
Raines, A ;
Hilton, T ;
Dessem, D .
JOURNAL OF COMPARATIVE NEUROLOGY, 2003, 460 (02) :167-179
[4]   Evolving the lock to fit the key to create a family of G protein-coupled receptors potently activated by an inert ligand [J].
Armbruster, Blaine N. ;
Li, Xiang ;
Pausch, Mark H. ;
Herlitze, Stefan ;
Roth, Bryan L. .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2007, 104 (12) :5163-5168
[5]   THE ROLE OF TRPA1 IN MUSCLE PAIN AND MECHANICAL HYPERSENSITIVITY UNDER INFLAMMATORY CONDITIONS IN RATS [J].
Asgar, J. ;
Zhang, Y. ;
Saloman, J. L. ;
Wang, S. ;
Chung, M. -K. ;
Ro, J. Y. .
NEUROSCIENCE, 2015, 310 :206-215
[6]   Restriction of Transient Receptor Potential Vanilloid-1 to the Peptidergic Subset of Primary Afferent Neurons Follows Its Developmental Downregulation in Nonpeptidergic Neurons [J].
Cavanaugh, Daniel J. ;
Chesler, Alexander T. ;
Braz, Joao M. ;
Shah, Nirao M. ;
Julius, David ;
Basbaum, Allan I. .
JOURNAL OF NEUROSCIENCE, 2011, 31 (28) :10119-10127
[7]   Trpv1 Reporter Mice Reveal Highly Restricted Brain Distribution and Functional Expression in Arteriolar Smooth Muscle Cells [J].
Cavanaugh, Daniel J. ;
Chesler, Alexander T. ;
Jackson, Alexander C. ;
Sigal, Yaron M. ;
Yamanaka, Hiroki ;
Grant, Rebecca ;
O'Donnell, Dajan ;
Nicoll, Roger A. ;
Shah, Nirao M. ;
Julius, David ;
Basbaum, Allan I. .
JOURNAL OF NEUROSCIENCE, 2011, 31 (13) :5067-5077
[8]   Distinct subsets of unmyelinated primary sensory fibers mediate behavioral responses to noxious thermal and mechanical stimuli [J].
Cavanaugh, Daniel J. ;
Lee, Hyosang ;
Lo, Liching ;
Shields, Shannon D. ;
Zylka, Mark J. ;
Basbaum, Allan I. ;
Anderson, David J. .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2009, 106 (22) :9075-9080
[9]   Roles of ASIC3, TRPV1, and NaV1.8 in the transition from acute to chronic pain in a mouse model of fibromyalgia [J].
Chen, Wei-Nan ;
Lee, Cheng-Han ;
Lin, Shing-Hong ;
Wong, Chia-Wen ;
Sun, Wei-Hsin ;
Wood, John N. ;
Chen, Chih-Cheng .
MOLECULAR PAIN, 2014, 10
[10]   Temporomandibular joint pain: A critical role for Trpv4 in the trigeminal ganglion [J].
Chen, Yong ;
Williams, Susan H. ;
McNulty, Amy L. ;
Hong, Ji Hee ;
Lee, Suk Hee ;
Rothfusz, Nicole E. ;
Parekh, Puja K. ;
Moore, Carlene ;
Gereau, Robert W. ;
Taylor, Andrea B. ;
Wang, Fan ;
Guilak, Farshid ;
Liedtke, Wolfgang .
PAIN, 2013, 154 (08) :1295-1304