385
Views
12
CrossRef citations to date
0
Altmetric
Research Article

Immunohistochemical Analysis of the Effects of Estrogen on Intraarticular Neurogenic Inflammation in a Rat Anterior Cruciate Ligament Transection Model of Osteoarthritis

, , , , , , & show all
Pages 197-206 | Received 30 May 2011, Accepted 26 Sep 2011, Published online: 05 Dec 2011

REFERENCES

  • Roach, H.I., Aigner, T., Soder, S., Haag, J., and Welkerling, H. (2007). Pathobiology of osteoarthritis: Pathomechanisms and potential therapeutic targets. Curr. Drug Targets 8:271–282.
  • Brandt, K.D., Radin, E.L., Dieppe, P.A., and van de Putte, L. (2006). Yet more evidence that osteoarthritis is not a cartilage disease. Ann. Rheum. Dis. 65:1261–1264.
  • Felson, D.T., and Zhang, Y. (1998). An update on the epidemiology of knee and hip osteoarthritis with a view to prevention. Arthritis Rheum. 41:1343–1355.
  • Smith, M.D., Triantafillou, S., Parker, A., Youssef, P.P., and Coleman, M. (1997). Synovial membrane inflammation and cytokine production in patients with early osteoarthritis. J. Rheumatol. 24:365–371.
  • Pearle, A.D., Scanzello, C.R., George, S., Mandl, L.A., DiCarlo, E.F., Peterson, M., Sculco, T.P., and Crow, M.K. (2007). Elevated high-sensitivity C-reactive protein levels are associated with local inflammatory findings in patients with osteoarthritis. Osteoarthr. Cartil. 15:516–523.
  • Bondeson, J., Wainwright, S.D., Lauder, S., Amos, N., and Hughes, C.E. (2006). The role of synovial macrophages and macrophage-produced cytokines in driving aggrecanases, matrix metalloproteinases, and other destructive and inflammatory responses in osteoarthritis. Arthritis Res. Ther. 8:R187.
  • Benito, M.J., Veale, D.J., FitzGerald, O., van den Berg, W.B., and Bresnihan, B. (2005). Synovial tissue inflammation in early and late osteoarthritis. Ann. Rheum. Dis. 64:1263–1267.
  • Goodstone, N.J., and Hardingham, T.E. (2002). Tumour necrosis factor alpha stimulates nitric oxide production more potently than interleukin-1beta in porcine articular chondrocytes. Rheumatology (Oxford) 41:883–891.
  • Levine, J.D., Clark, R., Devor, M., Helms, C., Moskowitz, M.A., and Basbaum, A.I. (1984). Intraneuronal substance P contributes to the severity of experimental arthritis. Science 226:547–549.
  • Marshall, K.W., Chiu, B., and Inman, R.D. (1990). Substance P and arthritis: Analysis of plasma and synovial fluid levels. Arthritis Rheum. 33:87–90.
  • Ahmed, M., Bjurholm, A., Schultzberg, M., Theodorsson, E., and Kreicbergs, A. (1995). Increased levels of substance P and calcitonin gene-related peptide in rat adjuvant arthritis. A combined immunohistochemical and radioimmunoassay analysis. Arthritis Rheum. 38:699–709.
  • Saito, T., and Koshino, T. (2000). Distribution of neuropeptides in synovium of the knee with osteoarthritis. Clin. Orthop. Relat. Res. 376:172–182.
  • Lembeck, F., and Holzer, P. (1979). Substance P as neurogenic mediator of antidromic vasodilation and neurogenic plasma extravasation. Naunyn. Schmiedebergs. Arch. Pharmacol. 310:175–183.
  • Nadkar, M.Y., Samant, R.S., Vaidya, S.S., and Borges, N.E. (1999). Relationship between osteoarthritis of knee and menopause. J. Assoc. Physicians India 47:1161–1163.
  • Roman-Blas, J.A., Castañeda, S., Largo, R., and Herrero-Beaumont, G. (2009). Osteoarthritis associated with estrogen deficiency. Arthritis Res. Ther. 11:241.
  • Hannan, M.T., Felson, D.T., Anderson, J.J., Naimark, A., and Kannel, W.B. (1990). Estrogen use and radiographic osteoarthritis of the knee in women. The Framingham Osteoarthritis Study. Arthritis Rheum. 33:525–532.
  • Spector, T.D., Nandra, D., Hart, D.J., and Doyle, D.V. (1997). Is hormone replacement therapy protective for hand and knee osteoarthritis in women? The Chingford Study. Ann. Rheum. Dis. 56:432–434.
  • Yang, Y., Ozawa, H., Lu, H., Yuri, K., Hayashi, S., Nihonyanagi, K., and Kawata, M. (1998). Immunocytochemical analysis of sex differences in calcitonin gene-related peptide in the rat dorsal root ganglion, with special reference to estrogen and its receptor. Brain Res. 791:35–42.
  • Kawamoto, T. (2003). Use of a new adhesive film for the preparation of multi-purpose fresh-frozen sections from hard tissues, whole-animals, insects and plants. Arch. Histol. Cytol. 66:123–143.
  • Yoshida, A., Morihara, T., Kajikawa, Y., Arai, Y., Oshima, Y., Kubo, T., Matsuda, K.I., Sakamoto, H., and Kawata, M. (2009). In vivo effects of ovarian steroid hormones on the expressions of estrogen receptors and the composition of extracellular matrix in the anterior cruciate ligament in rats. Connect. Tissue Res. 50:121–131.
  • Walsh, B.A., Mullick, A.E., Banka, C.E., and Rutledge, J.C. (2000). 17beta-estradiol acts separately on the LDL particle and artery wall to reduce LDL accumulation. J. Lipid Res. 41:134–141.
  • Stoop, R., Buma, P., van der Kraan, P.M., Hollander, A.P., Clark Billinghurst, R., Robin Poole, A., and van der Berg, W.B. (2000). Differences in type II collagen degradation between peripheral and central cartilage of rat stifle joints after cranial cruciate ligament transection. Arthritis Rheum. 43:2121–2131.
  • Sakamoto, H., Mezaki, Y., Shikimi, H., Ukena, K., and Tsutsui, K. (2003). Dendritic growth and spine formation in response to estrogen in the developing Purkinje cell. Endocrinology 144:4466–4477.
  • Kleemann, R.U., Krocker, D., Cedraro, A., Tuischer, J., and Duda, G.N. (2005). Altered cartilage mechanics and histology in knee osteoarthritis: Relation to clinical assessment (ICRS Grade). Osteoarthr. Cartil. 13:958–963.
  • Roselli, C.E., Thornton, J.E., and Chambers, K.C. (1993). Age-related deficits in brain estrogen receptors and sexual behavior of male rats. Behav. Neurosci. 107:202–209.
  • Stoop, R., Buma, P., van der Kraan, P.M., Hollander, A.P., Billinghurst, R.C., Meijers, T.H., Poole, A.R., and van der Berg, W.B. (2001). Type II collagen degradation in articular cartilage fibrillation after anterior cruciate ligament transection in rats. Osteoarthr. Cartil. 9:308–315.
  • Hayami, T., Pickarski, M., Zhuo, Y., Wesolowski, G.A., Rodan, G.A., and Duong, L.T. (2006). Characterization of articular cartilage and subchondral bone changes in the rat anterior cruciate ligament transection and meniscectomized models of osteoarthritis. Bone 38:234–243.
  • Gomez-Barrena, E., Nunez, A., Martinez-Moreno, E., Valls, J., and Munuera, L. (1997). Neural and muscular electric activity in the cat’s knee. Changes when the anterior cruciate ligament is transected. Acta. Orthop. Scand. 68:149–155.
  • Heppelmann, B., and Pawlak, M. (1997). Sensitisation of articular afferents in normal and inflamed knee joints by substance P in the rat. Neurosci. Lett. 223:97–100.
  • Ravn, P., Warming, L., Christgau, S., and Christiansen, C. (2004). The effect on cartilage of different forms of application of postmenopausal estrogen therapy: Comparison of oral and transdermal therapy. Bone 35:1216–1221.
  • Wluka, A.E., Wolfe, R., Davis, S.R., Stuckey, S., and Cicuttini, F.M. (2004). Tibial cartilage volume change in healthy postmenopausal women: A longitudinal study. Ann. Rheum. Dis. 63:444–449.
  • Cirillo, D.J., Wallace, R.B., Wu, L., and Yood, R.A. (2006). Effect of hormone therapy on risk of hip and knee joint replacement in the Women’s Health Initiative. Arthritis Rheum. 54:3194–3204.
  • Carbone, L.D., Nevitt, M.C., Wildy, K., Barrow, K.D., Harris, F., Felson, D., Paterfy, C., Visser, M., Harris, T.B., Wang, B.W., and Kritchevsky, S.B. (2004). The relationship of antiresorptive drug use to structural findings and symptoms of knee osteoarthritis. Arthritis Rheum. 50:3516–3525.
  • Taaffe, D.R., Sipila, S., Cheng, S., Puolakka, J., Toivanen, J., and Suominen, H. (2005). The effect of hormone replacement therapy and/or exercise on skeletal muscle attenuation in postmenopausal women: A yearlong intervention. Clin. Physiol. Funct. Imaging. 25:297–304.
  • Richardson, J.D., and Vasko, M.R. (2002). Cellular mechanisms of neurogenic inflammation. J. Pharmacol. Exp. Ther. 302:839–845.
  • Sohrabji, F., Miranda, R.C., and Toran-Allerand, C.D. (1994). Estrogen differentially regulates estrogen and nerve growth factor receptor mRNAs in adult sensory neurons. J. Neurosci. 14:459–471.
  • Williams, S.J., and Papka, R.E. (1996). Estrogen receptor-immunoreactive neurons are present in the female rat lumbosacral spinal cord. J. Neurosci. Res. 46:492–501.
  • Schaffer, M., Beiter, T., Becker, H.D., and Hunt, T.K. (1998). Neuropeptides: Mediators of inflammation and tissue repair? Arch. Surg. 133:1107–1116.
  • Levine, J.D., Khasar, S.G., and Green, P.G. (2006). Neurogenic inflammation and arthritis. Ann. N. Y. Acad. Sci. 1069:155–167.
  • Suri, S., Gill, S.E., de Camin, S.M., Wilson, D., McWilliams, D.F., and Walsh, D.A. (2007). Neurovascular invasion at the osteochondral junction and in osteophytes in osteoarthritis. Ann. Rheum. Dis. 66:1423–1428.
  • Imai, S., Tokunaga, Y., Maeda, T., Kikkawa, M., and Hukuda, S. (1997). Calcitonin gene-related peptide, substance P, and tyrosine hydroxylase-immunoreactive innervation of rat bone marrows: An immunohistochemical and ultrastructural investigation on possible efferent and afferent mechanisms. J. Orthop. Res. 15:133–140.
  • Niissalo, S., Hukkanen, M., Imai, S., Tornwall, J., and Konttinen, Y.T. (2002). Neuropeptides in experimental and degenerative arthritis. Ann. N. Y. Acad. Sci. 966:384–399.
  • Seegers, H.C., Hood, V.C., Kidd, B.L., Cruwys, S.C., and Walsh, D.A. (2003). Enhancement of angiogenesis by endogenous substance P release and neurokinin-1 receptors during neurogenic inflammation. J. Pharmacol. Exp. Ther. 306:8–12.
  • Nilsson, J., von Euler, A.M., and Dalsgaard, C.J. (1985). Stimulation of connective tissue cell growth by substance P and substance K. Nature 315:61–63.
  • Tanaka, T., Danno, K., Ikai, K., and Imamura, S. (1988). Effects of substance P and substance K on the growth of cultured keratinocytes. J. Invest. Dermatol. 90:399–401.
  • Lam, F.Y., and Ferrell, W.R. (1989). Inhibition of carrageenan induced inflammation in the rat knee joint by substance P antagonist. Ann. Rheum. Dis. 48:928–932.
  • Brain, S.D., and Williams, T.J. (1985). Inflammatory oedema induced by synergism between calcitonin gene-related peptide (CGRP) and mediators of increased vascular permeability. Br. J. Pharmacol. 86:855–860.
  • Schaible, H.G., Ebersberger, A., and Von Banchet, G.S. (2002). Mechanisms of pain in arthritis. Ann. N. Y. Acad. Sci. 966:343–354.
  • Zhang, L., Hoff, A.O., Wimalawansa, S.J., Cote, G.J., Gagel, R.F., and Westlund, K.N. (2001). Arthritic calcitonin/alpha calcitonin gene-related peptide knockout mice have reduced nociceptive hypersensitivity. Pain 89:265–273.
  • Walker, K.M., Urban, L., Medhurst, S.J., Patel, S., Panesar, M., Fox, A.J., and Mclntyre, P. (2003). The VR1 antagonist capsazepine reverses mechanical hyperalgesia in models of inflammatory and neuropathic pain. J. Pharmacol. Exp. Ther. 304:56–62.
  • Mapp, P.I., Kerslake, S., Brain, S.D., Blake, D.R., and Cambridge, H. (1996). The effect of intra-articular capsaicin on nerve fibres within the synovium of the rat knee joint. J. Chem. Neuroanat. 10:11–18.
  • Liu, B., Balkwill, A., Cooper, C., Brown, A., and Beral, V. (2009). Reproductive history, hormonal factors and the incidence of hip and knee replacement for osteoarthritis in middle-aged women. Ann. Rheum. Dis. 68:1165–1170.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.