Morphine suppresses tumor angiogenesis through a HIF-1α/p38MAPK pathway

American Journal of Pathology

Volumn 177, Issue 2, 2010, Pages 984-997

  Koodie, Lisa ^a   Ramakrishnan, Sundaram ^a   Roy, Sabita ^a  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1ALPHA; MITOGEN ACTIVATED PROTEIN KINASE P38; MITOGEN ACTIVATED PROTEIN KINASE P38 INHIBITOR; MORPHINE; NALTREXONE; OPIATE RECEPTOR; PLACEBO; VASCULOTROPIN;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CARCINOGENESIS; CARCINOMA CELL; CONTROLLED STUDY; DRUG BLOOD LEVEL; IN VITRO STUDY; LEWIS CARCINOMA; MORPHOMETRICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; RADIOIMMUNOASSAY; SLOW RELEASE FORMULATION; TUMOR CELL; TUMOR GROWTH;

EID: 77957275033     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.2353/ajpath.2010.090621     Document Type: Article

References (37)

1. Wiffen PJ, McQuay HJ: Oral morphine for cancer pain. Cochrane Database of Systematic Reviews 2007, 3:1-51
2. Cain DM, Wacnik PW, Eikmeier L, Beitz A, Wilcox G, Simone D: Functional interactions between tumor and peripheral nerve in a model of cancer pain in the mouse. Pain Med 2001, 2:15-23
3. Walsh D, Perin ML: Parenteral morphine prescribing patterns among inpatients with pain from advanced cancer: a prospective survey of intravenous and subcutaneous use. Am J Hosp Palliat Care Med 2006, 23:353-359
4. Aherne GW, Piall EM, Twycross RG: Serum morphine concentration after oral administration of diamorphine hydrochloride and morphine sulphate. Br J Clin Pharmacol 1979, 8:577-580
5. Tiseo PJ, Thaler HT, Lapin J, Inturrisi CE, Portenoy RK, Foley KM: Morphine-6-glucuronide concentrations and opioid-related side effects: a survey in cancer patients. Pain 1995, 61:47-54
6. Tegeder I, Grösch S, Schmidtko A: G protein-independent G1 cell cycle block and apoptosis with morphine in adenocarcinoma cells: involvement of p53 phosphorylation. Cancer Res 2003, 63:1846-1852
7. Gupta K, Kshirsagar S, Chang L, Schwartz R, Law PY, Yee D, Hebbel RP: Morphine stimulates angiogenesis by activating proangiogenic and survival-promoting signaling and promotes breast tumor growth. Cancer Res 2002, 62:4491-4498
8. Folkman J, D'Amore PA: Blood vessel formation: what is its molecular basis? Cell 1996, 87:1153-1155
9. Ferrara N: Vascular endothelial growth factor: basic science and clinical progress. Endocrine Rev 2004, 25:581-611
10. Brekken RA, Thorpe PE: Vascular endothelial growth factor and vascular targeting of solid tumors. Anticancer Res 2002, 21:4221-4229
11. Balsubramanian S, Ramakrishnan S, Charboneau R, Wang J, Roy S: Morphine sulfate inhibits hypoxia-induced vascular endothelial growth factor expression in endothelial cells and cardiac myocytes. J Mol Cell Cardiol 2001, 33:2179-2187
12. Blebea J, Mazo JE, Kihara TK, Vu JH, McLaughlin PJ, Atnip RG, Zagon IS: Opioid growth factor modulates angiogenesis. J Vasc Surg 2000, 32:364-373
13. Pasi A, Qu BX, Steiner R, Senn HJ, Bär W, Messiha FS: Angiogenesis: modulation with opioids. Gen Pharmacol 1991, 22:1077-1079
14. Liao D, Johnson RS: Hypoxia: a key regulator of angiogenesis in cancer. Cancer Metastasis Rev 2007, 26:281-290
15. Epstein AC, Gleadle JM, McNeill LA, Hewitson KS, O'Rourke J, Mole DR, Mukherji M, Metzen E, Wilson MI, Dhanda A, Tian YM, Masson N, Hamilton DL, Jaakkola P, Barstead R, Hodgkin J, Maxwell PH, Pugh CW, Schofield CJ, Ratcliffe PJ: Elegans EGL-9 and mammalian homologs define a family of dioxygenases that regulate HIF by prolyl hydroxylation. Cell 2001, 107(1):1-3
16. Minet E, Michel G, Mottet D: ERK activation upon hypoxia: involvement in HIF 1 activation. FEBS Lett 2000, 468:53-55
17. Richard DE, Berra E, Gothie E, Roux D, Pouyssegur J: p42/p44 mitogen-activated protein kinases phosphorylate hypoxia-inducible factor 1α (HIF-1α) and enhance the transcriptional activity of HIF-1. J Biol Chem 1999, 274:32631-32637
18. Sodhi A, Montaner S, Patel V, Zohar M, Bais C, Mesri EA, Gutkind JS: The Kaposi's sarcoma-associated herpes virus G protein-coupled receptor up-regulates vascular endothelial growth factor expression and secretion through mitogen-activated protein kinase and p38 pathways acting on hypoxia-inducible factor 1α. Cancer Res 2000, 60:4873-4880
19. Minet E, Michel G, Mottet D: Transduction pathways involved in Hypoxia-Inducible Factor-1 phosphorylation and activation. Free Radic Biol Med 2001, 31:847-855
20. Bilton R, Booker GW: The subtle side to hypoxia inducible factor (HIFα) regulation. Eur J of Biochem 2003, 270:791-798
21. Brancho D, Tanaka N, Jaeschke A, Ventura JJ, Kelkar N, Tanaka Y, Kyuuma M, Takeshita T, Flavell RA, Davis RJ: Mechanism of p38 MAP kinase activation in vivo. Genes Dev 2003, 17:1969-1978
22. Emerling BM, Platanias LC, Black E, Nebreda AR, Davis RJ, Chandel NS: Mitochondrial reactive oxygen species activation of p38 mitogen-activated protein kinase is required for hypoxia signaling. Mol Cell Biol 2005, 25:4853-4862
23. Singleton PA, Lingen MW, Fekete MJ, Garcia JG, Moss J: Methylnaltrexone inhibits opiate and VEGF-induced angiogenesis: role of receptor transactivation. Microvasc Res 2006, 72:3-11
24. Dussault AA, Pouliot M: Rapid and simple comparison of mRNA levels using real-time PCR. Biol Proceed Online 2006, 8:1-10
25. Wild R, Ramakrishnan S, Sedgewick J, Griffioen AW: Quantitative assessment of angiogenesis and tumor vessel architecture by computer-assisted digital image analysis: effects of VEGF-toxin conjugate on tumor microvessel density. Microvasc Res 2000, 59:368-376
26. Pasternak GW: The pharmacology of mu analgesics: from patients to genes. Neuroscientist 2001, 7:220-231
27. Pick CG, Nejat RJ, Pasternak GW: Independent expression of two pharmacologically distinct supraspinal mu analgesic systems in genetically different mouse strains. J Pharmacol Exp Ther 1993, 265:166-171
28. Lyden D, Hattori K, Dias S, Costa C, Blaikie P, Butros L, Chadburn A, Heissig B, Marks W, Witte L, Wu Y, Hicklin D, Zhu Z, Hackett NR, Crystal RG, Moore MA, Hajjar KA, Manova K, Benezra R, Rafii S: Impaired recruitment of bone-marrow-derived endothelial and hematopoietic precursor cells blocks tumor angiogenesis and growth. Nat Med 2001, 7:1194-1201
29. Barr MP, Bouchier-Hayes DJ, Harmey JJ: Vascular endothelial growth factor is an autocrine survival factor for breast tumour cells under hypoxia. Int J Oncol 2008, 32:41-48
30. Majamaa K, Günzler V, Hanauske-Abel HM, Myllylä R, Kivirikko KI: Partial identity of the 2-oxoglutarate and ascorbate binding sites of prolyl 4-hydroxylase. J Biol Chem 1986, 261:7819-7823
31. Sasaki T, Majamaa K, Uitto J: Reduction of collagen production in keloid fibroblast cultures by ethyl-3, 4-dihydroxybenzoate. Inhibition of prolyl hydroxylase activity as a mechanism of action J Biol Chem 1987, 262:9397-9403
32. Lee JW, Shahzad MM, Lin YG, Armaiz-Pena G, Mangala LS, Han HD, Kim HS, Nam EJ, Jennings NB, Halder J, Nick AM, Stone RL, Lu C, Lutgendorf SK, Cole SW, Lokshin AE, Sood AK: Surgical stress promotes tumor growth in ovarian carcinoma. Clin Cancer Res 2009, 15:2695-2702
33. Hermes GL, Delgado B, Tretiakova M, Cavigelli SA, Krausz T, Conzen SD, McClintock MK: Social isolation dysregulates endocrine and behavioral stress while increasing malignant burden of spontaneous mammary tumors. Proc Natl Acad Sci U S A 2009, 106:22393-22398
34. Micevych PE, Rissman EF, Gustafsson JA: Estrogen receptor-alpha is required for estrogen-induced mu-opioid receptor internalization. J Neurosci Res 2003, 71:802-810
35. Kisselev A, Goldberg A: Proteasome inhibitors: from research tools to drug candidates. Chem Biol 2001, 8:739-758
36. Kulisz A, Chen N, Chandel NS, Shao Z, Schumacker PT: Mitochondrial ROS initiate phosphorylation of p38 MAP kinase during hypoxia in cardiomyocytes. Am J Physiol Lung Cell Mol Physiol 2002, 282:L1324-L1329
37. Lin X, Li Q, Wang YJ, Ju YW, Chi ZQ, Wang MW, Liu JG: Morphine inhibits doxorubicin-induced reactive oxygen species generation and nuclear factor-kappaB transcriptional activation in neuroblastoma SH-SY5Y cells. Biochem J 2007, 406:215-221