The cystine/glutamate antiporter system xc- drives breast tumor cell glutamate release and cancer-induced bone pain

Pain

Volumn 157, Issue 11, 2016, Pages 2605-2616

  Slosky, Lauren M ^a   BassiriRad, Neemah M ^a   Symons, Ashley M ^a   Thompson, Michelle ^a   Doyle, Timothy ^a   Forte, Brittany L ^a   Staatz, William D ^a   Bui, Lynn ^a   Neumann, William L ^c   Mantyh, Patrick W ^a   Salvemini, Daniela ^b   Largent Milnes, Tally M ^a   Vanderah, Todd W ^a  

^a UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

^b SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c SOUTHERN ILLINOIS UNIVERSITY EDWARDSVILLE   (United States)

Author keywords

Cancer; Cystine glutamate antiporter; Glutamate; Nitrosative stress; Oxidative stress; Pain; Peroxynitrite; Reactive nitrogen species; Reactive oxygen species; Superoxide; Transporter

Indexed keywords

ANTIPORTER; CYSTINE GLUTAMATE ANTIPORTER SYSTEM XC; GLUTAMIC ACID; IRON MESO TETRAKIS (N METHYLPYRIDINIUM 4 YL)PORPHYRIN CHLORIDE; MANGANESE 5,15 DIPHENYL TETRACYCLOHEXENYLPORPHYIN CHLORIDE; PEROXYNITRITE; PORPHYRIN; SALAZOSULFAPYRIDINE; UNCLASSIFIED DRUG; 5,10,15,20-TETRAKIS(N-METHYL-4'-PYRIDYL)PORPHYRINATO-IRON(III); CALCIUM BINDING PROTEIN; METALLOPORPHYRIN; NONSTEROID ANTIINFLAMMATORY AGENT; PEROXYNITROUS ACID; SRI PROTEIN, MOUSE;

ADULT; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE METASTASIS; BONE PAIN; BREAST TUMOR; CANCER CELL LINE; CANCER PAIN; CONTROLLED STUDY; DRUG MECHANISM; ENZYME INHIBITION; ENZYME RELEASE; FEMALE; FEMUR; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPEATED DRUG DOSE; TUMOR CELL; TUMOR MICROENVIRONMENT; UPREGULATION; ADENOCARCINOMA; ANIMAL; BAGG ALBINO MOUSE; BONE TUMOR; COMPLICATION; DISEASE MODEL; DRUG EFFECTS; GENE EXPRESSION REGULATION; METABOLISM; PATHOLOGY; SECONDARY; TIME FACTOR; TUMOR CELL LINE; XENOGRAFT;

ADENOCARCINOMA; ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; ANTIPORTERS; BONE NEOPLASMS; BREAST NEOPLASMS; CALCIUM-BINDING PROTEINS; CANCER PAIN; CELL LINE, TUMOR; DISEASE MODELS, ANIMAL; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GLUTAMIC ACID; HETEROGRAFTS; METALLOPORPHYRINS; MICE; MICE, INBRED BALB C; PEROXYNITROUS ACID; SULFASALAZINE; TIME FACTORS;

EID: 84992630777     PISSN: 03043959     EISSN: 18726623     Source Type: Journal    
DOI: 10.1097/j.pain.0000000000000681     Document Type: Article

References (44)

1. American Cancer Society. Global Cancer Facts & Figures 2nd Edition. Atlanta: American Cancer Society; 2011.
2. Barclay JS, Owens JE, Blackhall LJ. Screening for substance abuse risk in cancer patients using the Opioid Risk Tool and urine drug screen. Support Care Cancer 2014;22:1883-8.
3. Bloom AP, Jimenez-Andrade JM, Taylor RN, Castaneda-Corral G, Kaczmarska MJ, Freeman KT, Coughlin KA, Ghilardi JR, Kuskowski MA, Mantyh PW. Breast cancer-induced bone remodeling, skeletal pain, and sprouting of sensory nerve fibers. J Pain 2011;12: 698-711.
4. Buckley BJ, Whorton AR. Adaptive responses to peroxynitrite: increased glutathione levels and cystine uptake in vascular cells. Am J Physiol Cell Physiol 2000;279:C1168-76.
5. Coleman RE. Metastatic bone disease: clinical features, pathophysiology and treatment strategies. Cancer Treat Rev 2001;27:165-76.
6. Coleman RE. Clinical features of metastatic bone disease and risk of skeletal morbidity. Clin Cancer Res 2006;12(20 pt 2):6243s-9s.
7. Coleman RE, Rubens RD. The clinical course of bone metastases from breast cancer. Br J Cancer 1987;55:61-6.
8. CurrieGL, Delaney A, Bennett MI, Dickenson AH, Egan KJ, VesterinenHM, Sena ES, MacleodMR, Colvin LA, FallonMT. Animalmodels of bone cancer pain: systematic review and meta-analyses. PAIN 2013;154:917-26.
9. Delaney A, Fleetwood-Walker SM, Colvin LA, Fallon M. Translational medicine: cancer pain mechanisms and management. Br J Anaesth 2008;101:87-94.
10. Denicola A, Souza JM, Radi R. Diffusion of peroxynitrite across erythrocyte membranes. Proc Natl Acad Sci U S A 1998;95:3566-71.
11. Dexter DL, Kowalski HM, Blazar BA, Fligiel Z, Vogel R, Heppner GH. Heterogeneity of tumor cells from a single mouse mammary tumor. Cancer Res 1978;38:3174-81.
12. Fisch MJ, Lee JW, Weiss M, Wagner LI, Chang VT, Cella D, Manola JB, Minasian LM, McCaskill-StevensW, Mendoza TR, CleelandCS. Prospective, observational study of pain and analgesic prescribing in medical oncology outpatients with breast, colorectal, lung, or prostate cancer. J Clin Oncol 2012;30:1980-8.
13. Flaherty KT, Puzanov I, Kim KB, Ribas A, McArthurGA, Sosman JA, O'Dwyer PJ, Lee RJ, Grippo JF, Nolop K, ChapmanPB. Inhibition of mutated, activated BRAF in metastatic melanoma. N Engl J Med 2010;363:809-19.
14. Ischiropoulos H. Biological tyrosine nitration: A pathophysiological function of nitric oxide and reactive oxygen species. Arch Biochem Biophys 1998;356:1-11.
15. Lewerenz J, Hewett SJ, Huang Y, Lambros M, Gout PW, Kalivas PW, Massie A, Smolders I, Methner A, Pergande M, Smith SB, Ganapathy V, Maher P. The cystine/glutamate antiporter system x(c)(-) in health and disease: from molecular mechanisms to novel therapeutic opportunities. Antioxid Redox Signal 2013;18:522-55.
16. Lozano-Ondoua AN, Hanlon KE, Symons-Liguori AM, Largent-Milnes TM, Havelin JJ, Ferland HL III, Chandramouli A, Owusu-Ankomah M, Nikolich-Zugich T, Bloom AP, Jimenez-Andrade JM, King T, Porreca F, Nelson MA, Mantyh PW, Vanderah TW. Disease modification of breast cancer-induced bone remodeling by cannabinoid 2 receptor agonists. J Bone Miner Res 2013;28:92-107.
17. Lozano-Ondoua AN, Symons-Liguori AM, Vanderah TW. Cancerinduced bone pain: mechanisms and models. Neurosci Lett 2013;(557 pt A):52-9.
18. Lozano-Ondoua AN, Wright C, Vardanyan A, King T, Largent-Milnes TM, Nelson M, Jimenez-Andrade JM, Mantyh PW, Vanderah TW. A cannabinoid 2 receptor agonist attenuates bone cancer-induced pain and bone loss. Life Sci 2010;86:646-53.
19. Lu T, Ramakrishnan R, Altiok S, Youn JI, Cheng P, Celis E, Pisarev V, Sherman S, Sporn MB, Gabrilovich D. Tumor-infiltrating myeloid cells induce tumor cell resistance to cytotoxic T cells in mice. J Clin Invest 2011;121:4015-29.
20. Mach DB, Rogers SD, Sabino MC, Luger NM, Schwei MJ, Pomonis JD, Keyser CP, Clohisy DR, Adams DJ, O'Leary P, Mantyh PW. Origins of skeletal pain: sensory and sympathetic innervation of the mouse femur. Neuroscience 2002;113:155-66.
21. Mercadante S. Malignant bone pain: pathophysiology and treatment. PAIN 1997;69:1-18.
22. Nagae M, Hiraga T, Yoneda T. Acidic microenvironment created by osteoclasts causes bone pain associatedwith tumor colonization. J Bone Miner Metab 2007;25:99-104.
23. Nakamura Y, Yasuoka H, Tsujimoto M, Yoshidome K, Nakahara M, Nakao K, Nakamura M, Kakudo K. Nitric oxide in breast cancer: induction of vascular endothelial growth factor-C and correlation with metastasis and poor prognosis. Clin Cancer Res 2006;12:1201-7.
24. O'Connell JX, Nanthakumar SS, Nielsen GP, Rosenberg AE. Osteoid osteoma: the uniquely innervated bone tumor. Mod Pathol 1998;11:175-80.
25. Pacher P, Beckman JS, Liaudet L. Nitric oxide and peroxynitrite in health and disease. Physiol Rev 2007;87:315-424.
26. Rausaria S, Ghaffari MM, Kamadulski A, Rodgers K, Bryant L, Chen Z, Doyle T, Shaw MJ, Salvemini D, Neumann WL. Retooling manganese(III) porphyrin-based peroxynitrite decomposition catalysts for selectivity and oral activity: A potential new strategy for treating chronic pain. J Med Chem 2011;54:8658-69.
27. Sabino MA, Mantyh PW. Pathophysiology of bone cancer pain. J Support Oncol 2005;3:15-24.
28. Salvemini D, Little JW, Doyle T, Neumann WL. Roles of reactive oxygen and nitrogen species in pain. Free Radic Biol Med 2011;51:951-66.
29. Salvemini D, Wang ZQ, Stern MK, Currie MG, Misko TP. Peroxynitrite decomposition catalysts: therapeutics for peroxynitrite-mediated pathology. Proc Natl Acad Sci U S A 1998;95:2659-63.
30. Sasaki H, Sato H, Kuriyama-Matsumura K, Sato K, Maebara K, Wang H, Tamba M, Itoh K, Yamamoto M, Bannai S. Electrophile response elementmediated induction of the cystine/glutamate exchange transporter gene expression. J Biol Chem 2002;277:44765-71.
31. Seidlitz EP, Sharma MK, Saikali Z, Ghert M, Singh G. Cancer cell lines release glutamate into the extracellular environment. Clin Exp Metastasis 2009;26:781-7.
32. Sharma MK, Seidlitz EP, Singh G. Cancer cells release glutamate via the cystine/glutamate antiporter. Biochem Biophys Res Commun 2010;391: 91-5.
33. Shukla K, Thomas AG, Ferraris DV, Hin N, Sattler R, Alt J, Rojas C, Slusher BS, Tsukamoto T. Inhibition of xc(-) transporter-mediated cystine uptake by sulfasalazine analogs. Bioorg Med Chem Lett 2011;21:6184-7.
34. Slosky LM, Largent-Milnes TM, Vanderah TW. Use of animal models in understanding cancer-induced bone pain. Cancer Growth Metastasis 2015;8(suppl 1):47-62.
35. Slosky LM, Vanderah TW. Therapeutic potential of peroxynitrite decomposition catalysts: A patent review. Expert Opin Ther Pat 2015; 25:443-66.
36. Tas F, Hansel H, Belce A, Ilvan S, Argon A, Camlica H, Topuz E. Oxidative stress in breast cancer. Med Oncology 2005;22:11-15.
37. Ungard RG, Seidlitz EP, Singh G. Oxidative stress and cancer pain. Can J Physiol Pharmacol 2013;91:31-7.
38. Ungard RG, Seidlitz EP, Singh G. Inhibition of breast cancer-cell glutamate release with sulfasalazine limits cancer-induced bone pain. PAIN 2014;155:28-36.
39. Vakkala M, Kahlos K, Lakari E, Paakko P, Kinnula V, Soini Y. Inducible nitric oxide synthase expression, apoptosis, and angiogenesis in in situ and invasive breast carcinomas. Clin Cancer Research 2000;6: 2408-16.
40. van den Beuken-van Everdingen MH, de Rijke JM, Kessels AG, Schouten HC, van Kleef M, Patijn J. Prevalence of pain in patients with cancer: A systematic review of the past 40 years. Ann Oncol 2007;18:1437-49.
41. Virag L, Szabo E, Gergely P, Szabo C. Peroxynitrite-induced cytotoxicity: mechanism and opportunities for intervention. Toxicol Lett 2003;140: 113-24.
42. Walser TC, Rifat S, Ma X, Kundu N, Ward C, Goloubeva O, Johnson MG, Medina JC, Collins TL, Fulton AM. Antagonism of CXCR3 inhibits lung metastasis in a murine model of metastatic breast cancer. Cancer Res 2006;66:7701-7.
43. Watkins LR, Wiertelak EP, Goehler LE, Smith KP, Martin D, Maier SF. Characterization of cytokine-induced hyperalgesia. Brain Res 1994;654: 15-26.
44. WHO. Cancer pain relief. Geneva, World Health Organziation, 1998.