Involvement of acidic microenvironment in the pathophysiology of cancer-associated bone pain

Bone

Volumn 48, Issue 1, 2011, Pages 100-105

  Yoneda, Toshiyuki ^a   Hata, Kenji ^a   Nakanishi, Masako ^a   Nagae, Maho ^a   Nagayama, Tomotaka ^a   Wakabayashi, Hiroki ^b   Nishisho, Toshihiko ^c   Sakurai, Teruhisa ^d   Hiraga, Toru ^e  

^a OSAKA UNIVERSITY   (Japan)

^b MIE UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c UNIVERSITY OF TOKUSHIMA   (Japan)

^d WAKAYAMA MEDICAL UNIVERSITY   (Japan)

^e MATSUMOTO DENTAL UNIVERSITY   (Japan)

Author keywords

Acid sensing nociceptors; Bisphosphonates; Dorsal root ganglion; Osteoclasts; Protons; Transient receptor potential channel vanilloid

Indexed keywords

ACID SENSING ION CHANNEL; BISPHOSPHONIC ACID DERIVATIVE; CALCITONIN GENE RELATED PEPTIDE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; VANILLOID RECEPTOR; VANILLOID RECEPTOR 1; ZOLEDRONIC ACID;

ACIDOSIS; BONE DESTRUCTION; BONE METASTASIS; BONE PAIN; CALCIUM TRANSPORT; CANCER PAIN; HUMAN; INFLAMMATION; NOCICEPTION; NONHUMAN; OSTEOCLAST; OSTEOPOROSIS; PATHOPHYSIOLOGY; REVIEW; SPINAL GANGLION;

ANIMALS; BONE AND BONES; BONE DENSITY CONSERVATION AGENTS; BONE NEOPLASMS; DIPHOSPHONATES; HUMANS; HYDROGEN-ION CONCENTRATION; INFLAMMATION; MODELS, ANIMAL; NEOPLASMS; NERVE TISSUE PROTEINS; NOCICEPTORS; OSTEOCLASTS; PAIN; PROTONS; SODIUM CHANNELS; TUMOR MICROENVIRONMENT;

EID: 78650305975     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2010.07.009     Document Type: Review

References (59)

1. Stucky C.L., Gold M.S., Zhang X. Mechanisms of pain. Proc Natl Acad Sci USA 2001, 98:11845-11846.
2. Bruela E., Kim H.N. Cancer pain 2003, 290:2476-2479.
3. Mercadante S. Malignant bone pain: pathophysiology and treatment. Pain 1997, 69:1-18.
4. Mantyh P.W., Clohisy D.R., Koltzenburg M., Hunt S. Molecular mechanism of cancer pain. Nature Rev. Cancer 2002, 2:201-209.
5. Julius D., Basbaum A.I. Molecular mechanism of nociception. Nature 2001, 413:203-210.
6. Jancso G., Kiraly E., Jancso-Gabor A. Pharmacologically induced selective degeneration of chemosensitive primary sensory neurons. Nature 1977, 270:741-743.
7. Saylor P.J., Smith M.R. Bone health and prostate cancer. Prostate Cancer Prostatic Dis 2010, 13:20-27.
8. Clohisy D.R., Mantyh P.W. Bone cancer pain. Cancer 2003, 97(3 suppl):866-873.
9. Pacharinsak C., Beitz A. Animal models of cancer pain. Comp Med 2008, 58:220-233.
10. Nagae M., Hiraga T., Yoneda T. Acidic microenvironment created by osteoclasts causes bone pain associated with tumor colonization. J Bone Miner Metab 2007, 25:99-104.
11. Hargreaves K., Dubner R., Brown F., Flores C., Joris J. A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain 1988, 32:77-88.
12. Honore P., Luger N.M., Sabino M.A.C., Schwei M.J., Rogers S.D., Mach D.B., O'keefe P.F., Ramnaraine M.L., Clohisy D.R., Mantyh P.W. Osteoprotegerin blocks bone cancer-induced skeletal destruction, skeletal pain and pain-related neurochemical reorganization of the spinal cord. Nature Med. 2000, 6:521-528.
13. Wacnik P.W., Kehl L.J., Trempe T.M., Ramnaraine M.L., Beitz A.J., Wilcox G.L. Tumor implantation in mouse humerus evokes movement-related hyperalgesia exceeding that evoked by intramuscular carrageenan. Pain 2003, 101:175-186.
14. Bove S.E., Calcaterra S.L., Brooker R.M., Huber C.M., Guzman R.E., Juneau P.L., Schrier D.J., Kilgore K.S. Weight bearing as a measure of disease progression and efficacy of anti-inflammatory compounds in a model of monosodium iodoacetate-induced osteoarthritis. Osteoarthritis Cartilage 2003, 11:821-830.
15. Wakabayashi H., Wakisaka S., Hiraga T., Sakurai, T., Tominaga M., Yoneda T. Role of acid-sensing TRPV1 in bone pain associated with cancer colonization in bone. J Bone Miner Res 2005, 20(Suppl 1):S32.
16. Hunt S.P., Pini A., Evan G. Induction of Fos-like protein in spinal cord neurons following sensory stimulation. Nature 1987, 328:632-634.
17. Obata K., Yamanaka H., Dai Y., Mizushima T., Fukuoka T., Tokunaga A., Noguchi K. Activation of extracellular signal-regulated protein kinase in the dorsal root ganglion following inflammation near the nerve cell body. Neuroscience 2004, 126:1011-1021.
18. Sango K., Horie H., Sotelo J.R., Takenaka T. A high glucose environment improves survival of diabetic neurons in culture. Neurosci Lett 1991, 129:277-280.
19. Nakanishi M., Hata K., Nagayama T., Sakurai T., Nishisho T., Wakabayashi H., Hiraga T., Ebisu S., Yoneda T. Acid activation of acid-sensing calcium channel Trpv1 leads to an up-regulation of calcitonin gene related peptide expression in dorsal root ganglion neurons via the CaMK-CREB cascade: a potential mechanism of inflammatory pain. Mol. Biol. Cell 2010, 30. doi/10.1091/mbc.E10-01-0049.
20. Nagae M., Hiraga T., Wakabayashi H., Wang L., Iwata K., Yoneda T. Osteoclasts play a part in pain due to the inflammation adjacent to bone. Bone 2006, 39:1107-1115.
21. Rousselle A.V., Heyman D. Osteoclast acidification pathways during bone resorption. Bone 2002, 30:535-540.
22. Griffiths J.R. Are cancer cells acidic?. Br J Cancer 1991, 64:425-427.
23. Gatenby R.A., Gawlinski E.T., Gmitro A.F., Kaylor B., Gillies R.J. Acid-mediated tumor invasion: a multidisciplinary study. Cancer Res 2006, 66:5216-5223.
24. Spugnini E.P., Citro G., Fais S. Proton pump inhibitors as anti vacuolar-ATPases drugs: a novel anticancer strategy. J Exp Clin Cancer Res 2010, 29:44.
25. Kedika R.R., Souza R.F., Spechler S.J. Potential anti-inflammatory effects of proton pump inhibitors: a review and discussion of the clinical implications. Dig Dis Sci 2009, 54:2312-2317.
26. Mach D.B., Rogers S.D., Sabino M.C., Luger N.M., Schwei M.J., Pomonis J.D., Keyser C.P., Clohisy D.R., Adams D.J., O'Leary P., Mantyh P.W. Origins of skeletal pain: sensory and sympathetic innervation of the mouse femur. Neuroiscience 2002, 113:155-166.
27. Szallasi A., Cortright D.N., Blum C.A., Eid S.R. The vanilloid receptor TRPV1: 10years from channel cloning to antagonist proof-of-concept. Nat Rev Drug Discov 2007, 6:357-372.
28. Caterina M.J., Schumacher M.A., Tominaga M., Rosen T.A., Levine J.D., Julius D. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 1997, 389:816-824.
29. Means A.R. Regulatory cascades involving calmodulin-dependent protein kinases. Mol Endocrinol 2000, 14:4-13.
30. Mellstrom B., Savignac M., Gomez-Villafuertes R., Naranjo J.R. Ca2+-operated transcriptional networks: molecular mechanisms and in vivo models. Physiol Rev 2008, 88:421-449.
31. Jara-Oseguera A., Simon S.A., Rosenbaum T. TRPV1: on the road to pain relief. Curr Mol Pharmacol 2008, 1:255-269.
32. Caterina M.J., Leffler A., Malmberg A.B., Martin W.J., Trafton J., Petersen-Zeitz K.R., Koltzenburg M., Basbaum A.I., Julius D. Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science 2000, 288:306-313.
33. Ghilardi J.R., Rohrich H., Lindsay T.H., Sevcik M.A., Schwei M.J., Kubota K., Halvorson K.G., Poblete J., Chaplan S.R., Dubin A.E., Carruthers N.I., Swanson D., Kuskowski M., Flores C.M., Julius D., Mantyh P.W. Selective blockade of the capsaicin receptor TRPV1 attenuates bone cancer pain. J Neurosci 2005, 25:3126-3131.
34. Krishtal O. The ASICs: signaling molecules? Modulators?. Trend Neuroscience 2003, 26:477-483.
35. White J.P., Cibelli M., Rei Fidalgo A., Paule C.C., Noormohamed F., Urban L., Maze M., Nagy I. Role of transient receptor potential and acid-sensing ion channels in peripheral inflammatory pain. Anesthesiology 2010, 112:729-741.
36. Voilley N., De Weille J., Mamet J., Lazdunski M. Nonsteroid anti-inflammatory drugs inhibit both the activity and the inflammation-induced expression of acid-sensing ion channels in nociceptors. J. Neuroscience 2001, 21:8026-8033.
37. Reeh P.W., Kress M. Molecular physiology of proton transduction in nociceptors. Curr Opin Pharmacol 2001, 1:45-51.
38. Ugawa S., Ueda T., Ishida Y., Nishigaki M., Shibata Y., Shimada S. Amiloride-blockable acid-sensing ion channels are leading acid sensors expressed in human nociceptors. J Clin Invest 2001, 110:1185-1190.
39. Olson T.H., Riede M.S., Vulchanova L., Ortiz-Gonzalez X.R., Elde R. An acid sensing ion channel (ASIC) localizes to small primary afferent neurons in rats. NeuroReport 1998, 1109-1113.
40. Hortobagyi G.N., Theriault R.L., Poter L., Blayney D., Lipton A., Sinoff C., Wheeler H., Simeone J.F., Seaman J., Knight R.D. Efficacy of pamidronate in reducing skeletal complications in patients with breast cancer and lytic bone metastases. N Engl J Med 1996, 335:1785-1791.
41. Fulfaro F., Casuccio A., Ticozzi C., Ripamonti C. The role of bisphosphonates in the treatment of painful metastatic bone disease: a review of phase III trials. Pain 1998, 78:157-169.
42. Lipton A., Theriault R.L., Hortobagyi G.N., Simeone J., Knight R.D., Mellars K., Reitsma D.J., Heffernan M., Seaman J.J. Pamidronate prevents skeletal complications and is effective palliative treatment in women with breast carcinoma and osteolytic bone metastases: long term follow-up of two randomized, placebo-controlled trials. Cancer 2000, 88:1082-1090.
43. Kohno N., Aogi K., Minami H., Nakamura S., Asaga T., Iino Y., Watanabe T., Goessl C., Ohashi Y., Takashima S. Zoledronic acid significantly reduces skeletal complications compared with placebo in Japanese women with bone metastases from breast cancer: a randomized, placebo-controlled trial. J Clin Oncol 2005, 23:3314-3321.
44. Francis R.M., Aspray T.J., Hide G., Sutcliffe A.M., Wilkinson P. Back pain in osteoporotic vertebral fractures. Osteoporos Int 2008, 19:895-903.
45. Luger N.M., Honore P., Sabino M.A., Schwei M.J., Rogers S.D., Mach D.B., Clohisy D.R., Mantyh P.W. Osteoprotegerin diminishes advanced bone cancer pain. Cancer Res 2001, 61:4038-4047.
46. Mundy G.R. Metastasis to bone: causes, consequences and therapeutic opportunities. Nature Rev. Cancer 2002, 2:584-593.
47. Roodman G.D. Mechanism of bone metastasis. N Engl J Med 2004, 350:1655-1664.
48. Yoneda T., Hiraga T. Crosstalk between cancer cells and bone microenvironment in bone metastasis. Biochem Biophys Res Commun 2005, 328:679-687.
49. Honore P., Rogers S.D., Schwell M.J., Salak-Johnson J.L., Luger N.M., Sabino M.C., Clohisy D.R., Mantyh P.W. Murine models of inflammatory, neuropathic and cancer pain each generates a unique set of neurochemical changes in the spinal cord and sensory neurons. Neuroscience 2000, 98:585-598.
50. Teitelbaum S.L. Bone resorption by osteoclasts. Science 2000, 289:1504-1508.
51. Boyle W.J., Simonet W.S., Lacey D.L. Osteoclast differentiation and activation. Nature 2003, 423:337-342.
52. Toyomura T., Murata Y., Yamamoto A., Oka T., Sun-Wada G.H., Wada Y., Futai M. From lysosomes to the plasma membrane: localization of vacuolar-type H+-ATPase with the a3 isoform during osteoclast differentiation. J Biol Chem 2003, 278:22023-22030.
53. Laitala T., Väänänen K. Proton channel part of vacuolar H+-ATPase and carbonic anhydrase II expression is stimulated in resorbing osteoclasts. J Bone Miner Res 1993, 8:119-126.
54. Visentin L., Dodds R.A., Valente M., Misiano P., Bradbeer J.N., Oneta S., Liang X., Gowen M., Farina C. A selective inhibitor of the osteoclastic V-H+-ATPase prevents bone loss in both thyroparathyroidectomized and ovariectomized rats. J Clin Invest 2000, 106:309-318.
55. Niikura K., Takano M., Sawada M. A novel inhibitor of vacuolar ATPase, FR167356, which can discriminate between osteoclast vacuolar ATPase and lysosomal vacuolar ATPase. Br J Pharmacol 2004, 142:558-566.
56. Martinez-Zaguilan R., Lynch R.M., Martinez G.M., Gilles R.J. Vacuolar-type H+-ATPases are functionally expressed in plasma membranes of human tumor cells. Amer. J. Physiol. 1993, 265:C1015-C1029.
57. Sennoune S.R., Bakunts K., Martinez G.M., Chua-Tuan J.L., Kebir Y., Attaya M.N., Martinez-Zaguilan R. Vacuolar H+-ATPase in human breast cancer cells with distinct metastatic potential: distribution and functional activity. Am J Physiol Cell Physiol 2004, 286:C1443-C1452.
58. Gillies R.J., Raghunand N., Karczmar G.S., Bhujwalla Z.M. MRI of the tumor microenvironment. J Magn Reson Imaging 2002, 16:430-450.
59. Lu X., Qin W., Li J., Tan N., Pan D., Zhang H., Xie L., Yao G., Shu H., Yao M., Wan D., Gu J., Yang S. The growth and metastasis of human hepatocellular carcinoma xenografts are inhibited by small interfering RNA targeting to the subunit ATP6L of proton pump. Cancer Res 2005, 65:6843-6849.