Endogenous opioid peptides, endomorphin-1 and -2 and deltorphin I, stimulate angiogenesis in the CAM assay

European Journal of Pharmacology

Volumn 579, Issue 1-3, 2008, Pages 269-275

  Dai, Xu ^a,b   Cui, Shi gang ^a,b   Wang, Ting ^a,b   Liu, Qian ^b   Song, Hong jin ^b   Wang, Rui ^a,b  

^a HONG KONG POLYTECHNIC UNIVERSITY   (Hong Kong)

^b School of Life Sciences   (China)

Author keywords

Angiogenesis; CAM; Deltorphin I; Endomorphin 1; Endomorphin 2

Indexed keywords

BASIC FIBROBLAST GROWTH FACTOR; DELTORPHIN; DELTORPHIN I; ENDOMORPHIN 1; ENDOMORPHIN 2; NALOXONE; UNCLASSIFIED DRUG;

ANGIOGENESIS; ANIMAL TISSUE; ARTICLE; CELL ASSAY; CHICK EMBRYO; CHORIOALLANTOIS; CONCENTRATION RESPONSE; CONTROLLED STUDY; EMBRYO; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION;

ANALGESICS, OPIOID; ANIMALS; CHICK EMBRYO; CHORIOALLANTOIC MEMBRANE; DOSE-RESPONSE RELATIONSHIP, DRUG; NALOXONE; NARCOTIC ANTAGONISTS; NEOVASCULARIZATION, PHYSIOLOGIC; OLIGOPEPTIDES; RECEPTORS, OPIOID, MU;

EID: 37549038311     PISSN: 00142999     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ejphar.2007.10.015     Document Type: Article

References (70)

1. Auerbach W., and Auerbach R. Angiogenesis inhibition: a review. Pharmacol Ther. 63 (1994) 265-311
2. Ausprunk D.H., Knighton D.R., and Folkman J. Differentiation of vascular endothelium in the chick chorioallantois: a structural and autoradiographic study. Dev Biol. 38 (1974) 237-248
3. Baumgartner I., Pieczek A., Manor O., Blair R., Kearney M., Walsh K., and Isner J.M. Constitutive expression of phVEGF165 after intramuscular gene transfer promotes collateral vessel development in patients with critical limb ischemia. Circulation 97 (1998) 1114-1123
4. Bertolucci M., Perego C., and De Simoni M.G. Central opiate modulation of peripheral IL-6 in rats. NeuroReport 7 (1996) 1181-1184
5. Blebea J., Mazo J.E., Kihara T.K., Vu J.H., McLaughlin P.J., Atnip R.G., and Zagon I.S. Opioid growth factor modulates angiogenesis. J. Vasc. Surg. 32 (2000) 364-373
6. Blebea J., Vu J.H., Assadnia S., McLaughlin P.J., Atnip R.G., and Zagon I.S. Differential effects of vascular growth factors on arterial and venous angiogenesis. J. Vasc. Surg. 35 (2002) 532-538
7. Bodnar R.J., and Klein G.E. Endogenous opiates and behavior: 2005. Peptides 27 (2006) 3391-3478
8. Cadet P., Bilfinger T.V., Fimiani C., Peter D., and Stefano G.B. Human vascular and cardiac endothelia express mu opiate receptor transcripts. Endothelium 7 (2000) 185-191
9. Cadet P., Mantione K.J., Bilfinger T.V., and Stefano G.B. Differential expression of the human mu opiate receptor from different primary vascular endothelial cells. Med. Sci. Monit. 10 (2004) BR351-BR355
10. Champion H.C., and Kadowitz P.J. D-[Ala2]endomorphin 2 and endomorphin 2 have nitric oxide-dependent vasodilator activity in rats. Am. J. Physiol. 274 (1998) H1690-H1697
11. Champion H.C., and Kadowitz P.J. Vasodepressor responses to [D-Ala2]-endomorphin 2 (TAPP) are mediated by an L-NAME-sensitive mechanism in the rat. J. Cardiovasc. Pharmacol. 33 (1999) 280-284
12. Chen C., Farooqui M., and Gupta K. Morphine stimulates vascular endothelial growth factor-like signaling in mouse retinal endothelial cells. Curr. Neurovasc. Res. 3 (2006) 171-180
13. Creamer D., Sullivan D., Bicknell R., and Barker J. Angiogenesis in psoriasis. Angiogenesis 5 (2002) 231-236
14. Crum R., Szabo S., and Folkman J. A new class of steroids inhibits angiogenesis in the presence of heparin or a heparin fragment. Science 230 (1985) 1375-1378
15. D'Amore P.A., and Thompson R.W. Mechanisms of angiogenesis. Annu. Rev. Physiol. 49 (1987) 453-464
16. Dhanabal M., Jeffers M., and Larochelle W.J. Anti-angiogenic therapy as a cancer treatment paradigm. Curr. Med. Chem. Anticancer Agents 5 (2005) 115-130
17. Ekstrand A.J., Cao R., Bjorndahl M., Nystrom S., Jonsson-Rylander A.C., Hassani H., Hallberg B., Nordlander M., and Cao Y. Deletion of neuropeptide Y (NPY) 2 receptor in mice results in blockage of NPY-induced angiogenesis and delayed wound healing. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 6033-6038
18. Fan T.P., Hu D.E., Guard S., Gresham G.A., and Watling K.J. Stimulation of angiogenesis by substance P and interleukin-1 in the rat and its inhibition by NK1 or interleukin-1 receptor antagonists. Br J Pharmacol. 110 (1993) 43-49
19. Fett J.W., Strydom D.J., Lobb R.R., Alderman E.M., Bethune J.L., Riordan J.F., and Vallee B.L. Isolation and characterization of angiogenin, an angiogenic protein from human carcinoma cells. Biochemistry 24 (1985) 5480-5486
20. Folkman J. Proceedings: tumor angiogenesis factor. Cancer Res. 34 (1974) 2109-2113
21. Folkman J. Tumor angiogenesis. Adv. Cancer Res. 43 (1985) 175-203
22. Folkman J. What is the evidence that tumors are angiogenesis dependent?. J. Natl. Cancer Inst. 82 (1990) 4-6
23. Folkman J. The role of angiogenesis in tumor growth. Semin. Cancer Biol. 3 (1992) 65-71
24. Folkman J. Clinical applications of research on angiogenesis. N. Engl. J. Med. 333 (1995) 1757-1763
25. Folkman J., and Shing Y. Angiogenesis. J. Biol. Chem. 267 (1992) 10931-10934
26. Geladopoulos T., Sakellaridis N., and Vernadakis A. Differential maturation of mu and delta opioid receptors in the chick embryonic brain. Neurochem. Res. 12 (1987) 279-288
27. Gibson D.A., and Vernadakis A. [3H]Etorphine binding activity in early chick embryos: brain and body tissue. Brain Res. 256 (1982) 23-29
28. Gupta K., Kshirsagar S., Chang L., Schwartz R., Law P.Y., Yee D., and Hebbel R.P. Morphine stimulates angiogenesis by activating proangiogenic and survival-promoting signaling and promotes breast tumor growth. Cancer Res. 62 (2002) 4491-4498
29. Hanahan D., and Folkman J. Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell 86 (1996) 353-364
30. Houghtling R.A., Mellon R.D., Tan R.J., and Bayer B.M. Acute effects of morphine on blood lymphocyte proliferation and plasma IL-6 levels. Ann. N. Y. Acad. Sci. 917 (2000) 771-777
31. Isner J.M., Pieczek A., Schainfeld R., Blair R., Haley L., Asahara T., Rosenfield K., Razvi S., Walsh K., and Symes J.F. Clinical evidence of angiogenesis after arterial gene transfer of phVEGF165 in patient with ischaemic limb. Lancet 348 (1996) 370-374
32. Kaliuzhnyi A.E., Platonov E.S., Mironova O.V., and Sukhikh G.T. Effects of opioids on the development of preimplantation mouse embryos. Biul. Ekspert. Biol. Med. 108 (1989) 622-624
33. Kalyuzhny A.E., Hensleigh H.C., Arvidsson U., and Elde R. Immunocytochemical localization of mu-opioid receptors in follicular cells and preimplantation mouse embryos. Anat. Embryol. (Berl) 195 (1997) 451-455
34. Kitlinska J., Abe K., Kuo L., Pons J., Yu M., Li L., Tilan J., Everhart L., Lee E.W., Zukowska Z., and Toretsky J.A. Differential effects of neuropeptide Y on the growth and vascularization of neural crest-derived tumors. Cancer Res. 65 (2005) 1719-1728
35. Klagsbrun M., and D'Amore P.A. Regulators of angiogenesis. Annu. Rev. Physiol. 53 (1991) 217-239
36. Kodani E., Xuan Y.T., Shinmura K., Takano H., Tang X.L., and Bolli R. Delta-opioid receptor-induced late preconditioning is mediated by cyclooxygenase-2 in conscious rabbits. Am. J. Physiol. Heart Circ. Physiol. 283 (2002) H1943-H1957
37. Krajnik M., Zylicz Z., Finlay I., Luczak J., and van Sorge A.A. Potential uses of topical opioids in palliative care-report of 6 cases. Pain 80 (1999) 121-125
38. Kuiper R.A., Schellens J.H., Blijham G.H., Beijnen J.H., and Voest E.E. Clinical research on antiangiogenic therapy. Pharmacol. Res. 37 (1998) 1-16
39. Kuwahara M.D., and Sparber S.B. Continuous exposure of the chick embryo to l-alpha-noracetylmethadol does not alter brain protein or nucleic acid content. Dev. Pharmacol. Ther. 3 (1981) 12-24
40. Lam C.F., Liu Y.C., Tseng F.L., Sung Y.H., Huang C.C., Jiang M.J., and Tsai Y.C. High-dose morphine impairs vascular endothelial function by increased production of superoxide anions. Anesthesiology 106 (2007) 532-537
41. Lazarous D.F., Shou M., Scheinowitz M., Hodge E., Thirumurti V., Kitsiou A.N., Stiber J.A., Lobo A.D., Hunsberger S., Guetta E., Epstein S.E., and Unger E.F. Comparative effects of basic fibroblast growth factor and vascular endothelial growth factor on coronary collateral development and the arterial response to injury. Circulation 94 (1996) 1074-1082
42. Leeson T.S., and Leeson C.R. The chorio-allantois of the chick. Light and electron microscopic observations at various times of incubation. J. Anat. 97 (1963) 585-595
43. Leong T.T., Fearon U., and Veale D.J. Angiogenesis in psoriasis and psoriatic arthritis: clues to disease pathogenesis. Curr. Rheumatol. Rep. 7 (2005) 325-329
44. Lin X., Yang D.J., Cai W.Q., Zhao Q.Y., Gao Y.F., Chen Q., and Wang R. Endomorphins, endogenous opioid peptides, provide antioxidant defense in the brain against free radical-induced damage. Biochim. Biophys. Acta 1639 (2003) 195-202
45. Neudeck B.L., and Loeb J.M. Endomorphin-1 alters interleukin-8 secretion in Caco-2 cells via a receptor mediated process. Immunol. Lett. 84 (2002) 217-221
46. Nguyen M., Shing Y., and Folkman J. Quantitation of angiogenesis and antiangiogenesis in the chick embryo chorioallantoic membrane. Microvasc. Res. 47 (1994) 31-40
47. Pal S., Wu J., Murray J.K., Gellman S.H., Wozniak M.A., Keely P.J., Boyer M.E., Gomez T.M., Hasso S.M., Fallon J.F., and Bresnick E.H. An antiangiogenic neurokinin-B/thromboxane A2 regulatory axis. J. Cell Biol. 174 (2006) 1047-1058
48. Papapetropoulos A., Garcia-Cardena G., Madri J.A., and Sessa W.C. Nitric oxide production contributes to the angiogenic properties of vascular endothelial growth factor in human endothelial cells. J. Clin. Invest. 100 (1997) 3131-3139
49. Pasi A., Qu B.X., Steiner R., Senn H.J., Bar W., and Messiha F.S. Angiogenesis: modulation with opioids. Gen Pharmacol. 22 (1991) 1077-1079
50. Poonawala T., Levay-Young B.K., Hebbel R.P., and Gupta K. Opioids heal ischemic wounds in the rat. Wound Repair Regen. 13 (2005) 165-174
51. Qi Y.M., Yang D.J., Duan X., Yang F., Li S.R., Shen J.M., and Wang R. Endomorphins inhibit contractile responses of rat thoracic aorta rings induced by phenylephrine and angiotensin II in vitro. Acta Pharmacol Sin. 23 (2002) 40-44
52. Ribatti D., Conconi M.T., and Nussdorfer G.G. Nonclassic endogenous regulators of angiogenesis. Pharmacol Rev. 59 (2007) 185-205
53. Ribatti D., Gualandris A., Bastaki M., Vacca A., Iurlaro M., Roncali L., and Presta M. New model for the study of angiogenesis and antiangiogenesis in the chick embryo chorioallantoic membrane: the gelatin sponge/chorioallantoic membrane assay. J Vasc Res. 34 (1997) 455-463
54. Rogers P.A., Abberton K.M., and Susil B. Endothelial cell migratory signal produced by human endometrium during the menstrual cycle. Hum Reprod. 7 (1992) 1061-1066
55. Rosengart T.K., Lee L.Y., Patel S.R., Sanborn T.A., Parikh M., Bergman G.W., Hachamovitch R., Szulc M., Kligfield P.D., Okin P.M., Hahn R.T., Devereux R.B., Post M.R., Hackett N.R., Foster T., Grasso T.M., Lesser M.L., Isom O.W., and Crystal R.G. Angiogenesis gene therapy: phase I assessment of direct intramyocardial administration of an adenovirus vector expressing VEGF121 cDNA to individuals with clinically significant severe coronary artery disease. Circulation. 100 (1999) 468-474
56. Seegers H.C., Hood V.C., Kidd B.L., Cruwys S.C., and Walsh D.A. Enhancement of angiogenesis by endogenous substance P release and neurokinin-1 receptors during neurogenic inflammation. J Pharmacol Exp Ther. 306 (2003) 8-12
57. Singleton P.A., Lingen M.W., Fekete M.J., Garcia J.G., and Moss J. Methylnaltrexone inhibits opiate and VEGF-induced angiogenesis: role of receptor transactivation. Microvasc. Res. 72 (2006) 3-11
58. Stefano G.B., Salzet M., Hughes T.K., and Bilfinger T.V. Delta2 opioid receptor subtype on human vascular endothelium uncouples morphine stimulated nitric oxide release. Int. J. Cardiol. 64 Suppl 1 (1998) S43-S51
59. Stefano G.B., Neenan K., Cadet P., Magazine H., and Bilfinger T.V. Ischemic preconditioning - an opiate constitutive nitric oxide molecular hypothesis. Med. Sci. Monit. 7 (2001) 1357-1375
60. Takeshita S., Weir L., Chen D., Zheng L.P., Riessen R., Bauters C., Symes J.F., Ferrara N., and Isner J.M. Therapeutic angiogenesis following arterial gene transfer of vascular endothelial growth factor in a rabbit model of hindlimb ischemia. Biochem. Biophys. Res. Commun. 227 (1996) 628-635
61. Tsurumi Y., Kearney M., Chen D., Silver M., Takeshita S., Yang J., Symes J.F., and Isner J.M. Treatment of acute limb ischemia by intramuscular injection of vascular endothelial growth factor gene. Circulation 96 9 Suppl (1997) II-382-388
62. Twillman R.K., Long T.D., Cathers T.A., and Mueller D.W. Treatment of painful skin ulcers with topical opioids. J. Pain Symp. Manage. 17 (1999) 288-292
63. Wakabayashi Y., Shono T., Isono M., Hori S., Matsushima K., Ono M., and Kuwano M. Dual pathways of tubular morphogenesis of vascular endothelial cells by human glioma cells: vascular endothelial growth factor/basic fibroblast growth factor and interleukin-8. Jpn. J. Cancer Res. 86 (1995) 1189-1197
64. Watkins L.R., Maier S.F., and Goehler L.E. Immune activation: the role of pro-inflammatory cytokines in inflammation, illness responses and pathological pain states. Pain 63 (1995) 289-302
65. Weinstat-Saslow D., and Steeg P.S. Angiogenesis and colonization in the tumor metastatic process: basic and applied advances. FASEB J. 8 (1994) 401-407
66. Wilting J., Christ B., and Bokeloh M. A modified chorioallantoic membrane (CAM) assay for qualitative and quantitative study of growth factors. Studies on the effects of carriers, PBS, angiogenin, and bFGF. Anat. Embryol. (Berl). 183 (1991) 259-271
67. Worthen D.M., Fenton B.M., Rosen P., and Zweifach B. Morphometry of diabetic conjunctival blood vessels. Ophthalmology 88 (1981) 655-657
68. Wu N., Ren W.H., Huo X.F., Chen Q., and Wang R. Effects of endomorphins and their analogs on cardiovascular system. Yao Xue Xue Bao 36 (2001) 241-245
69. Ziche M., Jones J., and Gullino P.M. Role of prostaglandin E1 and copper in angiogenesis. J. Natl. Cancer Inst. 69 (1982) 475-482
70. Ziche M., Morbidelli L., Choudhuri R., Zhang H.T., Donnini S., Granger H.J., and Bicknell R. Nitric oxide synthase lies downstream from vascular endothelial growth factor-induced but not basic fibroblast growth factor-induced angiogenesis. J. Clin. Invest. 99 (1997) 2625-2634