Angiotensin II receptor type 2 activation is required for cutaneous sensory hyperinnervation and hypersensitivity in a rat hind paw model of inflammatory Pain

Journal of Pain

Volumn 14, Issue 10, 2013, Pages 1053-1065

  Chakrabarty, Anuradha ^a,b   Liao, Zhaohui ^a,b   Smith, Peter G ^a,b  

^a UNIVERSITY OF KANSAS MEDICAL CENTER   (United States)

^b UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

Author keywords

dorsal root ganglion; Mechanical allodynia; nociceptors; sprouting; thermal sensitivity

Indexed keywords

1 (4 DIMETHYLAMINO 3 METHYLBENZYL) 5 DIPHENYLACETYL 4,5,6,7 TETRAHYDRO 1H IMIDAZO[4,5 C]PYRIDINE 6 CARBOXYLIC ACID; ANGIOTENSIN RECEPTOR; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR RECEPTOR; GNDF FAMILY RECEPTOR ALPHA 2; NEUROFILAMENT H PROTEIN; TYROSINE 3 MONOOXYGENASE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEMALE; HYPERSENSITIVITY; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INFLAMMATORY PAIN; MACROPHAGE; NERVE FIBER; NEUROFILAMENT; NONHUMAN; PAW EDEMA; RAT; SKIN NERVE; T LYMPHOCYTE;

DORSAL ROOT GANGLION; MECHANICAL ALLODYNIA; NOCICEPTORS; SPROUTING; THERMAL SENSITIVITY;

ANGIOTENSIN II TYPE 1 RECEPTOR BLOCKERS; ANIMALS; BEHAVIOR, ANIMAL; FEMALE; FOOT; FREUND'S ADJUVANT; HINDLIMB; HOT TEMPERATURE; HYPERALGESIA; IMIDAZOLES; INFLAMMATION; NEURONAL PLASTICITY; PHYSICAL STIMULATION; PYRIDINES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, ANGIOTENSIN, TYPE 2; RENIN-ANGIOTENSIN SYSTEM; SENSORY RECEPTOR CELLS; SKIN;

EID: 84885018016     PISSN: 15265900     EISSN: 15288447     Source Type: Journal    
DOI: 10.1016/j.jpain.2013.04.002     Document Type: Article

References (83)

1. A.A. Al-Majed, C.M. Neumann, T.M. Brushart, and T. Gordon Brief electrical stimulation promotes the speed and accuracy of motor axonal regeneration J Neurosci 20 2000 2602 2608
2. K.M. Albers, C.J. Woodbury, A.M. Ritter, B.M. Davis, and H.R. Koerber Glial cell line-derived neurotrophic factor expression in skin alters the mechanical sensitivity of cutaneous nociceptors J Neurosci 26 2006 2981 2990
3. H. Alfredson, L. Ohberg, and S. Forsgren Is vasculo-neural ingrowth the cause of pain in chronic Achilles tendinosis? An investigation using ultrasonography and colour Doppler, immunohistochemistry, and diagnostic injections Knee Surg Sports Traumatol Arthrosc 11 2003 334 338
4. L. Almarestani, G. Longo, and A. Ribeiro-da-Silva Autonomic fiber sprouting in the skin in chronic inflammation Mol Pain 4 2008 56
5. A.M. Aloisi, and R.B. Fillingim Sensory effects of gonadal hormones Sex, Gender, and Pain 2000 IASP Press Seattle, WA 7
6. M. Alterman Development of selective non-peptide angiotensin II type 2 receptor agonists J Renin Angiotensin Aldosterone Syst 11 2010 57 66
7. U. Anand, P. Facer, Y. Yiangou, M. Sinisi, M. Fox, T. McCarthy, C. Bountra, Y.E. Korchev, and P. Anand Angiotensin II type 2 receptor (AT(2) R) localization and antagonist-mediated inhibition of capsaicin responses and neurite outgrowth in human and rat sensory neurons Eur J Pain 2012 [Epub ahead of print]
8. S. Beggs, D. Alvares, A. Moss, G. Currie, J. Middleton, M.W. Salter, and M. Fitzgerald A role for NT-3 in the hyperinnervation of neonatally wounded skin Pain 153 2012 2133 2139
9. J.A. Black, S. Liu, M. Tanaka, T.R. Cummins, and S.G. Waxman Changes in the expression of tetrodotoxin-sensitive sodium channels within dorsal root ganglia neurons in inflammatory pain Pain 108 2004 237 247
10. A.D. Blacklock, J.A. Cauveren, and P.G. Smith Estrogen selectively increases sensory nociceptor innervation of arterioles in the female rat Brain Res 1018 2004 55 65
11. A.D. Blacklock, M.S. Johnson, D. Krizsan-Agbas, and P.G. Smith Estrogen increases sensory nociceptor neuritogenesis in vitro by a direct, nerve growth factor-independent mechanism Eur J Neurosci 21 2005 2320 2328
12. A.D. Blacklock, and P.G. Smith Estrogen increases calcitonin gene-related peptide-immunoreactive sensory innervation of rat mammary gland J Neurobiol 59 2004 192 204
13. N. Bohm-Starke, M. Hilliges, C. Falconer, and E. Rylander Increased intraepithelial innervation in women with vulvar vestibulitis syndrome Gynecol Obstet Invest 46 1998 256 260
14. N. Bohm-Starke, M. Hilliges, C. Falconer, and E. Rylander Neurochemical characterization of the vestibular nerves in women with vulvar vestibulitis syndrome Gynecol Obstet Invest 48 1999 270 275
15. N. Bohm-Starke, and E. Rylander Surgery for localized, provoked vestibulodynia: A long-term follow-up study J Reprod Med 53 2008 83 89
16. M.F. Brown, M.V. Hukkanen, I.D. McCarthy, D.R. Redfern, J.J. Batten, H.V. Crock, S.P. Hughes, and J.M. Polak Sensory and sympathetic innervation of the vertebral endplate in patients with degenerative disc disease J Bone Joint Surg 79 1997 147 153
17. A.S. Burris, R.H. Gracely, C.S. Carter, R.J. Sherins, and J.M. Davidson Testosterone therapy is associated with reduced tactile sensitivity in human males Horm Behav 25 1991 195 205
18. A. Chakrabarty, A. Blacklock, S. Svojanovsky, and P.G. Smith Estrogen elicits dorsal root ganglion axon sprouting via a renin-angiotensin system Endocrinology 149 2008 3452 3460
19. A. Chakrabarty, K.E. McCarson, and P.G. Smith Hypersensitivity and hyperinnervation of the rat hind paw following carrageenan-induced inflammation Neurosci Lett 495 2011 67 71
20. J. Constantinou, M.L. Reynolds, C.J. Woolf, B. Safieh-Garabedian, and M. Fitzgerald Nerve growth factor levels in developing rat skin: Upregulation following skin wounding NeuroReport 5 1994 2281 2284
21. C.D. Cook, and K.I. Moore Effects of sex, hindpaw injection site and stimulus modality on nociceptive sensitivity in arthritic rats Physiol Behav 87 2006 552 562
22. F. Cote, T.H. Do, L. Laflamme, J.M. Gallo, and N. Gallo-Payet Activation of the AT(2) receptor of angiotensin II induces neurite outgrowth and cell migration in microexplant cultures of the cerebellum J Biol Chem 274 1999 31686 31692
23. R.M. Craft Modulation of pain by estrogens Pain 132 Suppl 1 2007 S3 S12
24. I.N. Day, and R.J. Thompson UCHL1 (PGP 9.5): Neuronal biomarker and ubiquitin system protein Prog Neurobiol 90 2010 327 362
25. P. Di Sebastiano, T. Fink, E. Weihe, H. Friess, H.G. Beger, and M. Buchler Changes of protein gene product 9.5 (PGP 9.5) immunoreactive nerves in inflamed appendix Dig Dis Sci 40 1995 366 372
26. S.D. Dib-Hajj, J. Fjell, T.R. Cummins, Z. Zheng, K. Fried, R. LaMotte, J.A. Black, and S.G. Waxman Plasticity of sodium channel expression in DRG neurons in the chronic constriction injury model of neuropathic pain Pain 83 1999 591 600
27. A.L.N. Doss, and P.G. Smith Nerve-langerhans cell interactions in diabetes and aging Histol Histopathol 27 2012 1589 1598
28. M.A. Farmer, A.M. Taylor, A.L. Bailey, A.H. Tuttle, L.C. Macintyre, Z.E. Milagrosa, H.P. Crissman, G.J. Bennett, A. Ribeiro-da-Silva, Y.M. Binik, and J.S. Mogil Repeated vulvovaginal fungal infections cause persistent pain in a mouse model of vulvodynia Sci Transl Med 3 2011 101ra191
29. R.B. Fillingim, T.J. Ness, and R.B. Fillingim The influence of menstrual cycle and sex hormones on pain responses in humans Sex, Gender, and Pain. Progress in Pain Research and Management Volume 17 2000 IASP Press Seattle 191
30. S.L. Forrest, and J.R. Keast Expression of receptors for glial cell line-derived neurotrophic factor family ligands in sacral spinal cord reveals separate targets of pelvic afferent fibers J Comp Neurol 506 2008 989 1002
31. G. Gaunt, A. Good, and C.R. Stanhope Vestibulectomy for vulvar vestibulitis J Reprod Med 48 2003 591 595
32. L. Gendron, L. Laflamme, N. Rivard, C. Asselin, M.D. Payet, and N. Gallo-Payet Signals from the AT2 (angiotensin type 2) receptor of angiotensin II inhibit p21ras and activate MAPK (mitogen-activated protein kinase) to induce morphological neuronal differentiation in NG108-15 cells Mol Endocrinol 13 1999 1615 1626
33. M.F. Goetsch Simplified surgical revision of the vulvar vestibule for vulvar vestibulitis Am J Obstet Gynecol 174 1996 1701 1705 discussion 1705-1707
34. P. Gopinath, E. Wan, A. Holdcroft, P. Facer, J.B. Davis, G.D. Smith, C. Bountra, and P. Anand Increased capsaicin receptor TRPV1 in skin nerve fibres and related vanilloid receptors TRPV3 and TRPV4 in keratinocytes in human breast pain BMC Womens Health 5 2005 2
35. L. Grossmann, N. Gorodetskaya, A. Teliban, R. Baron, and W. Janig Cutaneous afferent C-fibers regenerating along the distal nerve stump after crush lesion show two types of cold sensitivity Eur J Pain 13 2009 682 690
36. M.O. Guimond, C. Roberge, and N. Gallo-Payet Fyn is involved in angiotensin II type 2 receptor-induced neurite outgrowth, but not in p42/p44mapk in NG108-15 cells Mol Cell Neurosci 45 2010 201 212
37. M. Hanssens, L. Vercruysse, M.J. Keirse, R. Pijnenborg, and F.A. Van Assche Identification of "renin"-containing cells in the choriodecidua Placenta 16 1995 517 525
38. K. Hargreaves, R. Dubner, F. Brown, C. Flores, and J. Joris A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia Pain 32 1988 77 88
39. N.E. Hoch, T.J. Guzik, W. Chen, T. Deans, S.A. Maalouf, P. Gratze, C. Weyand, and D.G. Harrison Regulation of T-cell function by endogenously produced angiotensin II Am J Physiol Regul Integr Comp Physiol 296 2009 R208 R216
40. S.T. Hsieh, G.J. Kidd, T.O. Crawford, Z. Xu, W.M. Lin, B.D. Trapp, D.W. Cleveland, and J.W. Griffin Regional modulation of neurofilament organization by myelination in normal axons J Neurosci 14 1994 6392 6401
41. H. Imboden, J. Patil, J. Nussberger, F. Nicoud, B. Hess, N. Ahmed, T. Schaffner, M. Wellner, D. Muller, T. Inagami, T. Senbonmatsu, J. Pavel, and J.M. Saavedra Endogenous angiotensinergic system in neurons of rat and human trigeminal ganglia Regul Pept 154 2009 23 31
42. W. Janig, L. Grossmann, and N. Gorodetskaya Mechano- and thermosensitivity of regenerating cutaneous afferent nerve fibers Exp Brain Res 196 2009 101 114
43. C. Janse, B. Peretz, M. van der Roest, and E.J. Dubelaar Excitability and branching of neuroendocrine cells during reproductive senescence Neurobiol Aging 20 1999 675 683
44. C.I. Johnston Franz Volhard Lecture. Renin-angiotensin system: A dual tissue and hormonal system for cardiovascular control J Hypertension Suppl 10 1992 S13 S26
45. M. Jurewicz, D.H. McDermott, J.M. Sechler, K. Tinckam, A. Takakura, C.B. Carpenter, E. Milford, and R. Abdi Human T and natural killer cells possess a functional renin-angiotensin system: Further mechanisms of angiotensin II-induced inflammation J Am Soc Nephrol 18 2007 1093 1102
46. L.M. Kow, and D.W. Pfaff Effects of estrogen treatment on the size of receptive field and response threshold of pudendal nerve in the female rat Neuroendocrinology 13 1973 299 313
47. A.A. Larson, D.R. Brown, S. el-Atrash, and M.M. Walser Pain threshold changes in adjuvant-induced inflammation: A possible model of chronic pain in the mouse Pharmacol Biochem Behav 24 1986 49 53
48. R. Lucius, S. Gallinat, P. Rosenstiel, T. Herdegen, J. Sievers, and T. Unger The angiotensin II type 2 (AT2) receptor promotes axonal regeneration in the optic nerve of adult rats J Exp Med 188 1998 661 670
49. L.M. Lundberg, P. Alm, J. Wharton, and J.M. Polak Protein gene product 9.5 (PGP 9.5). A new neuronal marker visualizing the whole uterine innervation and pregnancy-induced and developmental changes in the guinea pig Histochemistry 90 1988 9 17
50. M. Macova, J. Pavel, and J.M. Saavedra A peripherally administered, centrally acting angiotensin II AT2 antagonist selectively increases brain AT1 receptors and decreases brain tyrosine hydroxylase transcription, pituitary vasopressin and ACTH Brain Res 1250 2009 130 140
51. S.A. Malin, D.C. Molliver, H.R. Koerber, P. Cornuet, R. Frye, K.M. Albers, and B.M. Davis Glial cell line-derived neurotrophic factor family members sensitize nociceptors in vitro and produce thermal hyperalgesia in vivo J Neurosci 26 2006 8588 8599
52. S. Manivannan, and S. Terakawa Rapid sprouting of filopodia in nerve terminals of chromaffin cells, PC12 cells, and dorsal root neurons induced by electrical stimulation J Neurosci 14 1994 5917 5928
53. E.S. McCoy, B. Taylor-Blake, and M.J. Zylka CGRPalpha-expressing sensory neurons respond to stimuli that evoke sensations of pain and itch PloS One 7 2012 e36355
54. M.J. McKinley, A.L. Albiston, A.M. Allen, M.L. Mathai, C.N. May, R.M. McAllen, B.J. Oldfield, F.A. Mendelsohn, and S.Y. Chai The brain renin-angiotensin system: Location and physiological roles Int J Biochem Cell Biol 35 2003 901 918
55. K. Micklem, E. Rigney, J. Cordell, D. Simmons, P. Stross, H. Turley, B. Seed, and D. Mason A human macrophage-associated antigen (CD68) detected by six different monoclonal antibodies Br J Haematol 73 1989 6 11
56. M.J. Iadarola, L.S. Brady, G. Draisci, and R. Dubner Enhancement of dynorphin gene expression in spinal cord following experimental inflammation: Stimulus specificity, behavioral parameters and opioid receptor binding Pain 35 1988 313 326
57. D.C. Molliver, D.E. Wright, M.L. Leitner, A.S. Parsadanian, K. Doster, D. Wen, Q. Yan, and W.D. Snider IB4-binding DRG neurons switch from NGF to GDNF dependence in early postnatal life Neuron 19 1997 849 861
58. Y. Nagakura, M. Okada, A. Kohara, T. Kiso, T. Toya, A. Iwai, F. Wanibuchi, and T. Yamaguchi Allodynia and hyperalgesia in adjuvant-induced arthritic rats: Time course of progression and efficacy of analgesics J Pharmacol Exp Ther 306 2003 490 497
59. R.L. Nahin, and M.R. Byers Adjuvant-induced inflammation of rat paw is associated with altered calcitonin gene-related peptide immunoreactivity within cell bodies and peripheral endings of primary afferent neurons J Comp Neurol 349 1994 475 485
60. J. Patil, A. Schwab, J. Nussberger, T. Schaffner, J.M. Saavedra, and H. Imboden Intraneuronal angiotensinergic system in rat and human dorsal root ganglia Regul Pept 162 2010 90 98
61. D.M. Pechlivanova, P.P. Markova, D. Popov, and A.G. Stoynev The role of the angiotensin AT2 receptor on the diurnal variations of nociception and motor coordination in rats Peptides 39 2013 152 156
62. J.C. Petruska, and L.M. Mendell The many functions of nerve growth factor: Multiple actions on nociceptors Neurosci Lett 361 2004 168 171
63. K. Reinecke, R. Lucius, A. Reinecke, U. Rickert, T. Herdegen, and T. Unger Angiotensin II accelerates functional recovery in the rat sciatic nerve in vivo: Role of the AT2 receptor and the transcription factor NF-kappaB FASEB J 17 2003 2094 2096
64. J.L. Riley 3rd, M.E. Robinson, E.A. Wise, and D.D. Price A meta-analytic review of pain perception across the menstrual cycle Pain 81 1999 225 235
65. T. Sakagawa, S. Okuyama, N. Kawashima, S. Hozumi, O. Nakagawasai, T. Tadano, K. Kisara, T. Ichiki, and T. Inagami Pain threshold, learning and formation of brain edema in mice lacking the angiotensin II type 2 receptor Life Sci 67 2000 2577 2585
66. V. Sanchis-Alfonso, and E. Rosello-Sastre Immunohistochemical analysis for neural markers of the lateral retinaculum in patients with isolated symptomatic patellofemoral malalignment. A neuroanatomic basis for anterior knee pain in the active young patient Am J Sports Med 28 2000 725 731
67. V. Sanchis-Alfonso, E. Rosello-Sastre, C. Monteagudo-Castro, and J. Esquerdo Quantitative analysis of nerve changes in the lateral retinaculum in patients with isolated symptomatic patellofemoral malalignment. A preliminary study Am J Sports Med 26 1998 703 709
68. J. Sandkühler Models and mechanisms of hyperalgesia and allodynia Physiol Rev 89 2009 707 758
69. R. Sanoja, and F. Cervero Estrogen-dependent changes in visceral afferent sensitivity Auton Neurosci 153 2010 84 89
70. T.E. Schubert, C. Weidler, K. Lerch, F. Hofstadter, and R.H. Straub Achilles tendinosis is associated with sprouting of substance P positive nerve fibres Ann Rheum Dis 64 2005 1083 1086
71. P.G. Smith, M. George, and S. Bradshaw Estrogen promotes sympathetic nerve regeneration in rat proximal urethra Urology 73 2009 1392 1396
72. S.E. Tague, G.L. Clarke, M.K. Winter, K.E. McCarson, D.E. Wright, and P.G. Smith Vitamin D deficiency promotes skeletal muscle hypersensitivity and sensory hyperinnervation J Neurosci 31 2011 13728 13738
73. H.C. Tai, and E.M. Schuman Ubiquitin, the proteasome and protein degradation in neuronal function and dysfunction Nat Rev Neurosci 9 2008 826 838
74. L. Tanzer, and K.J. Jones Gonadal steroid regulation of hamster facial nerve regeneration: Effects of dihydrotestosterone and estradiol Exp Neurol 146 1997 258 264
75. A.M. Taylor, J.C. Peleshok, and A. Ribeiro-da-Silva Distribution of P2X(3)-immunoreactive fibers in hairy and glabrous skin of the rat J Comp Neurol 514 2009 555 566
76. A.Y. Ting, A.D. Blacklock, and P.G. Smith Estrogen regulates vaginal sensory and autonomic nerve density in the rat Biol Reprod 71 2004 1397 1404
77. P. Tympanidis, G. Terenghi, and P. Dowd Increased innervation of the vulval vestibule in patients with vulvodynia Br J Dermatol 148 2003 1021 1027
78. J.V. Weinstock, and A.M. Blum Granuloma macrophages in murine schistosomiasis mansoni generate components of the angiotensin system Cell Immunol 89 1984 39 45
79. K.D. Wilkinson, K. Lee, S. Deshpande, P. Duerksen-Hughes, J.M. Boss, and J. Pohl The neuron-specific protein PGP 9.5 is a ubiquitin carboxyl-terminal hydrolase Science 246 1989 670 673
80. C.J. Woolf Generation of acute pain: Central mechanisms Br Med Bull 47 1991 523 533
81. C.J. Woolf, and Q. Ma Nociceptors - Noxious stimulus detectors Neuron 55 2007 353 364
82. Y.H. Zhang, J. Kays, K.E. Hodgdon, T.C. Sacktor, and G.D. Nicol Nerve growth factor enhances the excitability of rat sensory neurons through activation of the atypical protein kinase C isoform, PKMzeta J Neurophysiol 107 2012 315 335
83. M. Zimmermann, and T. Herdegen Plasticity of the nervous system at the systematic, cellular and molecular levels: A mechanism of chronic pain and hyperalgesia Prog Brain Res 110 1996 233 259 Development