Morphine stimulates vascular endothelial growth factor-like signaling in mouse retinal endothelial cells

Current Neurovascular Research

Volumn 3, Issue 3, 2006, Pages 171-180

  Chen, Chunsheng ^a   Farooqui, Mariya ^a   Gupta, Kalpna ^a  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

Author keywords

FLR KDR; G protein coupled receptors; MAPK ERK; Mu opioid receptor; PDGFR; Receptor tyrosine kinase; STAT3; Transactivation

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; MORPHINE; MU OPIATE RECEPTOR; PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR; PROTEIN KINASE B; RNA; STAT3 PROTEIN; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 2;

ANGIOGENESIS; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL ISOLATION; CELL PROLIFERATION; CELL SURVIVAL; CELL TRANSPORT; CONTROLLED STUDY; DRUG EFFECT; DRUG MECHANISM; ENDOTHELIUM CELL; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; IMMUNOPRECIPITATION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RECEPTOR UPREGULATION; RETINA CELL; SIGNAL TRANSDUCTION;

ANALGESICS, OPIOID; ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CELL PROLIFERATION; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOTHELIAL CELLS; FLUORESCENT ANTIBODY TECHNIQUE; IMMUNOPRECIPITATION; MICE; MICE, INBRED C57BL; MITOGEN-ACTIVATED PROTEIN KINASES; MORPHINE; ORGAN CULTURE TECHNIQUES; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTOR, PLATELET-DERIVED GROWTH FACTOR BETA; RECEPTORS, OPIOID, MU; RETINAL VESSELS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; TRANS-ACTIVATION (GENETICS); VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 33746893866     PISSN: 15672026     EISSN: None     Source Type: Journal    
DOI: 10.2174/156720206778018767     Document Type: Article

References (43)

1. Aicher, A, Heeschen, C, Mildner-Rihm, C, Urbich, C, Ihling, C, Technau-Ihling, K, Zeiher, AM, Dimmeler, S. (2003) Essential role of endothelial nitric oxide synthase for mobilization of stem and progenitor cells. Nat Med 9: 1370-1376.
2. Ando, A, Yang, A, Mori, K, Yamada, H, Yamada, E, Takahashi, K, Saikia, J, Kim, M, Melia, M, Fishman, M, Huang, P, Campochiaro, PA. (2002) Nitric oxide is proangiogenic in the retina and choroid. J Cell Physiol 191: 116-124.
3. Balasubramanian, S, Ramakrishnan, S, Charboneau, R, Wang, J, Barke, RA, Roy, S. (2001) Morphine sulfate inhibits hypoxia-induced vascular endothelial growth factor expression in endothelial cells and cardiac myocytes. J Mol Cell Cardiol 33: 2179-2187.
4. Bartoli, M, Gu, X, Tsai, NT, Venema, RC, Brooks, SE, Marrero, MB, Caldwell, RB. (2000) Vascular endothelial growth factor activates stat proteins in aortic endothelial cells. J Biol Chem 275: 33189-33192.
5. Bartoli, M, Platt, D, Lemtalsi, T, Gu, X, Brooks, SE, Marrero, MB, Caldwell, RB. (2003) VEGF differentially activates STAT3 in microvascular endothelial cells. FASEB J 17: 1562-1564.
6. Belcheva, MM, Szucs, M, Wang, D, Sadee, W, Coscia, CJ. (2001) Muopioid receptor-mediated ERK activation involves calmodulin-dependent epidermal growth factor receptor transactivation. J Biol Chem 276: 33847-33853.
7. Belcheva, MM, Haas, PD, Tan, Y, Heaton, VM, Coscia, CJ. (2002) The fibroblast growth factor receptor is at the site of convergence between mu-opioid receptor and growth factor signaling pathways in rat c6 glioma cells. J Pharmacol Exp Ther 303: 909-918.
8. Blebea, J, Mazo, JE, Kihara, TK, Vu, J-H, McLaughlin, PJ, Atnip, RG, Zagon, IS. (2000) Opioid growth factor modulates angiogenesis. J Vasc Surg 32: 364-373.
9. Chang, SL, Moldow, RL, Wu, G-d, Vidal, EL, Patel, NA. (1998) The association between opiates and cytokines. Adv Exp Med Biol 437: 4-6.
10. Dauer, DJ, Ferraro, B, Song, L, Yu, B, Mora, L, Buettner, R, Enkemann, S, Jove, R, Haura, EB. (2005) Stat3 regulates genes common to both wound healing and cancer. Oncogene 24: 3397-3408.
11. Duh, E, Aiello, LP. (1999) Vascular endothelial growth factor and diabetes: The agonist versus antagonist paradox. Diabetes 48: 1899-1906.
12. Dvorak, HF, Detmar, M, Claffey, KP, Nagy, JA, van de Water, L, Senger, DR. (1995) Vascular permeability factor/vascular endothelial growth factor: An important mediator of angiogenesis in malignancy and inflammation. Int Arch Allergy Immunol 107: 233-235.
13. Farooqui, M, Geng, ZH, Stephenson, EJ, Zaveri, N, Yee, D, Gupta, K. (2006) Naloxone acts as an antagonist of estrogen receptor activity in MCF-7 cells. Mol Cancer Ther 5: 611-620.
14. Feng, Y, Venema, VJ, Venema, RC, Tsai, N, Caldwell, RB. (1999) VEGF induces nuclear translocation of Flk-1/KDR, endothelial nitric oxide synthase, and caveolin-1 in vascular endothelial cells. Biochem Biophys Res Commun 256: 192-197.
15. Ferrara, N, Davis-Smyth, T. (1997) The biology of vascular endothelial growth factor. Endocr Rev 18: 4-25.
16. Ferrara, N. (2002) VEGF and the quest for tumour angiogenesis factors. Nat Rev Cancer 2: 795-803.
17. Fukumura, D, Gohongi, T, Kadambi, A, Izumi, Y, Ang, J, Yun, CO, Buerk, DG, Huang, PL, Jain, RK. (2001) Predominant role of endothelial nitric oxide synthase in vascular endothelial growth factor-induced angiogenesis and vascular permeability. Proc Natl Acad Sci USA 98: 2604-2609.
18. Gerber, HP, Malik, AK, Solar, GP, Sherman, D, Liang, XH, Meng, G, Hong, K, Marsters, JC, Ferrara, N. (2002) VEGF regulates haematopoietic stem cell survival by an internal autocrine loop mechanism. Nature 417: 954-958.
19. Grisshammer, R, Tate, CG. (1995) Overexpression of integral membrane proteins for structural studies. Q Rev Biophys 28: 315-422.
20. Gupta, K, Ramakrishnan, S, Browne, PV, Solovey, A, Hebbel, RP. (1997) A novel technique for culture of human dermal microvascular endothelial cells under either serum-free or serum-supplemented conditions: Isolation by panning and stimulation with vascular endothelial growth factor. Exp Cell Res 230: 244-251.
21. Gupta, K, Kshirsagar, S, Chang, L, Schwartz, R, Law, PY, Yee, D, Hebbel, RP. (2002) Morphine stimulates angiogenesis by activating proangiogenic and survival-promoting signaling and promotes breast tumor growth. Cancer Res 62: 4491-4498.
22. Guthrie, SM, Curtis, LM, Mames, RN, Simon, GG, Grant, MB, Scott, EW. (2005) The nitric oxide pathway modulates hemangioblast activity of adult hematopoietic stem cells. Blood 105: 1916-1922.
23. Hellewell, SB, Bowen, WD. (1990) A sigma-like binding site in rat pheochromocytoma (pc12) cells: Decreased affinity for (+)-benzomorphans and lower molecular weight suggest a different sigma receptor form from that of guinea pig brain. Brain Res 527: 244-253.
24. Johnson, HM, Torres, BA, Green, MM, Szente, BE, Siler, KI, Larkin, J, 3rd, Subramaniam, PS. (1998) Cytokine-receptor complexes as chaperones for nuclear translocation of signal transducers. Biochem Biophys Res Commun 244: 607-614.
25. Klepstad, P, Kaasa, S, Borchgrevink, PC. (2000) Start of oral morphine to cancer patients: Effective serum morphine concentrations and contribution from morphine-6-glucuronide to the analgesia produced by morphine. Eur J Clin Pharmacol 55: 713-719.
26. Kroll, J, Waltenberger, J. (1997) The vascular endothelial growth factor receptor KDR activates multiple signal transduction pathways in porcine aortic endothelial cells. J Biol Chem 272: 32521-32527.
27. McQuay, HJ, Carroll, D, Faura, CC, Gavaghan, DJ, Hand, CW, Moore, RA. (1990) Oral morphine in cancer pain: Influences on morphine and metabolite concentration. Clin Pharmacol Ther 48: 236-244.
28. Murohara, T, Asahara, T, Silver, M, Bauters, C, Masuda, H, Kalka, C, Kearney, M, Chen, D, Symes, JF, Fishman, MC, Huang, PL, Isner, JM. (1998) Nitric oxide synthase modulates angiogenesis in response to tissue ischemia. J Clin Invest 101: 2567-2578.
29. Pasi, Q, Qu, BX, Steiner, R, Senn, HJ, Bar, W, and Messiha, FS. (1991) Angiogenesis: modulation with opioids. Gen Pharmacol 22: 1077-1079.
30. Poonawala, T, Levay-Young, BK, Hebbel, RP, Gupta, K. (2005) Opioids heal ischemic wounds in the rat. Wound Repair Regen 13: 165-174.
31. Sarramegna, V, Muller, I, Mousseau, G, Froment, C, Monsarrat, B, Milon, A, Talmont, F. (2005) Solubilization, purification, and mass spectrometry analysis of the human mu-opioid receptor expressed in pichia pastoris. Protein Expr Purif 43: 85-93.
32. Stefano, GB, Hartman, A, Bilfinger, TV, Magazine, HI, Liu, Y, Casares, F, Goligorsky, MS. (1995) Presence of the mu3 opiate receptor in endothelial cells. Coupling to nitric oxide production and vasodilation. J Biol Chem 270: 30290-30293.
33. Stephenson, EJ, Martinez-Suarez, HJ, Farooqui, M, Mukhopadhyay, D, Hughes, DA, Mukherjee, P, Gupta, K. (2005) μ Opioid receptor stimulates a growth promoting and pro-angiogenic tumor microenvironment by transactivating VEGF Receptor-2/Flk-1. Blood 106: 3687.
34. Tanimoto, T, Jin, ZG, Berk, BC. (2002) Transactivation of vascular endothelial growth factor (VEGF) receptor Flk-1/KDR is involved in sphingosine 1-phosphate-stimulated phosphorylation of Akt and endothelial nitric-oxide synthase (ENOS). J Biol Chem 277: 42997-43001.
35. Tegeder, I, Geisslinger, G. (2004) Opioids as modulators of cell death and survival - unraveling mechanisms and revealing new indications. Pharmacol Rev 56: 351-369.
36. Tryoen-Toth, P, Gaveriaux-Ruff, C, Maderspach, K, Labourdette, G. (1998) Regulation of kappa-opioid receptor mRNA level by cyclic AMP and growth factors in cultured rat glial cells. Brain Res Mol Brain Res 55: 141-150.
37. Waldhoer, M, Bartlett, SE, Whistler, JL. (2004) Opioid receptors. Annu Rev Biochem 73: 953-990.
38. Wang, Z, Bilsky, EJ, Porreca, F, Sadee, W. (1994) Constitutive mu opioid receptor activation as a regulatory mechanism underlying narcotic tolerance and dependence. Life Sci 54: PL339-350.
39. Wetzker, R, Bohmer, FD. (2003) Transactivation joins multiple tracks to the ERK/MAPK cascade. Nat Rev Mol Cell Biol 4: 651-657.
40. Zeng, H, Zhao, D, Mukhopadhyay, D. (2002) KDR stimulates endothelial cell migration through heterotrimeric G protein Gq/11-mediated activation of a small GTPase RhoA. J Biol Chem 277: 46791-46798.
41. Zeng, H, Zhao, D, Yang, S, Datta, K, Mukhopadhyay, D. (2003) Heterotrimeric G alpha q/G alpha 11 proteins function upstream of vascular endothelial growth factor (VEGF) receptor-2 (KDR) phosphorylation in vascular permeability factor/VEGF signaling. J Biol Chem 278: 20738-20745.
42. Ziche, M, Morbidelli, L, Masini, E, Amerini, S, Granger, HJ, Maggi, CA, Geppetti, P, Ledda, F. (1994) Nitric oxide mediates angiogenesis in vivo and endothelial cell growth and migration in vitro promoted by substance P. J Clin Invest 94: 2036-2044.
43. Ziche, M, Morbidelli, L, Choudhuri, R, Zhang, HT, Donnini, S, Granger, HJ, Bicknell, R. (1997) Nitric oxide synthase lies downstream from vascular endothelial growth factor-induced but not basic fibroblast growth factor-induced angiogenesis. J Clin Invest 99: 2625-2634.