Dopamine stabilizes tumor blood vessels by up-regulating angiopoietin 1 expression in pericytes and Krüppel-like factor-2 expression in tumor endothelial cells

Proceedings of the National Academy of Sciences of the United States of America

Volumn 108, Issue 51, 2011, Pages 20730-20735

  Chakroborty, Debanjan ^a   Sarkar, Chandrani ^a   Yu, Hongmei ^a   Wang, Jiang ^b   Liu, Zhongfa ^a,b   Dasgupta, Partha Sarathi ^c   Basu, Sujit ^a,b  

^a OHIO STATE UNIVERSITY   (United States)

^b OHIO STATE UNIVERSITY   (United States)

^c CHITTARANJAN NATIONAL CANCER INSTITUTE   (India)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOPOIETIN 1; DOPAMINE; DOPAMINE 2 RECEPTOR; DOPAMINE 2 RECEPTOR STIMULATING AGENT; FLUOROURACIL; KRUPPEL LIKE FACTOR 2; NEUROTRANSMITTER; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; ZINC FINGER TRANSCRIPTIONAL FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; COLON CANCER; CONTROLLED STUDY; DRUG EFFICACY; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PERICYTE; PRIORITY JOURNAL; PROSTATE TUMOR; PROTEIN EXPRESSION; RECEPTOR UPREGULATION; SYMPATHETIC INNERVATION; TUMOR CELL; TUMOR ENDOTHELIUM CELL; TUMOR VASCULARIZATION; ZINC FINGER MOTIF;

ANGIOPOIETIN-1; ANIMALS; ANOXIA; ANTINEOPLASTIC AGENTS; BLOOD VESSELS; CELL LINE, TUMOR; DOPAMINE; ENDOTHELIAL CELLS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MICE; MICROSCOPY, CONFOCAL; NEOVASCULARIZATION, PATHOLOGIC; PERICYTES; UP-REGULATION;

EID: 84862952645     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1108696108     Document Type: Article

References (57)

1. Jain RK (2005) Normalization of tumor vasculature: An emerging concept in antiangiogenic therapy. Science 307:58-62.
2. Fukumura D, Duda DG, Munn LL, Jain RK (2010) Tumor microvasculature and microenvironment: Novel insights through intravital imaging in pre-clinical models. Microcirculation 17:206-225.
3. Hamzah J, et al. (2008) Vascular normalization in Rgs5-deficient tumours promotes immune destruction. Nature 453:410-414. (Pubitemid 351693122)
4. Hanahan D, Folkman J (1996) Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell 86:353-364. (Pubitemid 26272076)
5. Engerman RL, Pfaffenbach D, Davis MD (1967) Cell turnover of capillaries. Lab Invest 17:738-743.
6. Hobson B, Denekamp J (1984) Endothelial proliferation in tumours and normal tissues: Continuous labelling studies. Br J Cancer 49:405-413. (Pubitemid 14125248)
7. Heath VL, Bicknell R (2009) Anticancer strategies involving the vasculature. Nat Rev Clin Oncol 6:395-404.
8. Missale C, Nash SR, Robinson SW, Jaber M, Caron MG (1998) Dopamine receptors: From structure to function. Physiol Rev 78:189-225. (Pubitemid 28070979)
9. Rubí B, Maechler P (2010) Minireview: New roles for peripheral dopamine on metabolic control and tumor growth: Let's seek the balance. Endocrinology 151:5570-5581.
10. Sarkar C, Basu B, Chakroborty D, Dasgupta PS, Basu S (2010) The immunoregulatory role of dopamine: An update. Brain Behav Immun 24:525-528.
11. Tsuru H, Tanimitsu N, Hirai T (2002) Role of perivascular sympathetic nerves and regional differences in the features of sympathetic innervation of the vascular system. Jpn J Pharmacol 88:9-13. (Pubitemid 34139832)
12. Carmeliet P (2003) Blood vessels and nerves: Common signals, pathways and diseases. Nat Rev Genet 4:710-720.
13. Krimer LS, Muly EC, 3rd, Williams GV, Goldman-Rakic PS (1998) Dopaminergic regulation of cerebral cortical microcirculation. Nat Neurosci 1:286-289.
14. De Backer D, et al.; SOAP II Investigators (2010) Comparison of dopamine and norepinephrine in the treatment of shock. N Engl J Med 362:779-789.
15. Zeng C, Zhang M, Asico LD, Eisner GM, Jose PA (2007) The dopaminergic system in hypertension. Clin Sci (Lond) 112:583-597. (Pubitemid 46849549)
16. Li ZS, Pham TD, Tamir H, Chen JJ, Gershon MD (2004) Enteric dopaminergic neurons: Definition, developmental lineage, and effects of extrinsic denervation. J Neurosci 24:1330-1339. (Pubitemid 38222983)
17. Tsukamoto K, et al. (2005) Projections to the alimentary canal from the dopaminergic neurons in the dorsal motor nucleus of the vagus of the rat. Auton Neurosci 123:12-18. (Pubitemid 41736133)
18. Katzung BG (2009) Anatomy of the Autonomic Nervous System, eds Katzung BG, Masters SB, Trevor AJ (McGraw-Hill, New York), p 78.
19. Amenta F, Ricci A, Tayebati SK, Zaccheo D (2002) The peripheral dopaminergic system: Morphological analysis, functional and clinical applications. Ital J Anat Embryol 107:145-167.
20. Tayebati SK, Lokhandwala MF, Amenta F (2011) Dopamine and vascular dynamics control: Present status and future perspectives. Curr Neurovasc Res 8:246-257.
21. Davies MA, et al. (2002) Adenoviral-mediated expression of MMAC/PTEN inhibits proliferation and metastasis of human prostate cancer cells. Clin Cancer Res 8:1904-1914. (Pubitemid 34633753)
22. Morikawa K, Walker SM, Jessup JM, Fidler IJ (1988) In vivo selection of highly metastatic cells from surgical specimens of different primary human colon carcinomas implanted into nude mice. Cancer Res 48:1943-1948.
23. Burt AD, et al. (1989) Localization of adrenergic and neuropeptide tyrosine-containing nerves in the mammalian liver. Hepatology 9:839-845. (Pubitemid 19140088)
24. Miller LE, Jüsten HP, Schölmerich J, Straub RH (2000) The loss of sympathetic nerve fibers in the synovial tissue of patients with rheumatoid arthritis is accompanied by increased norepinephrine release from synovial macrophages. FASEB J 14:2097-2107.
25. Liang CS, Yatani A, Himura Y, Kashiki M, Stevens SY (2002) Desipramine attenuates loss of cardiac sympathetic neurotransmitters produced by congestive heart failure and NE infusion. Am J Physiol Heart Circ Physiol 282:H363-H371.
26. Kanazawa H, et al. (2010) Heart failure causes cholinergic transdifferentiation of cardiac sympathetic nerves via gp130-signaling cytokines in rodents. J Clin Invest 120:408-421.
27. Eldrup E, Richter EA (2000) DOPA, dopamine, and DOPAC concentrations in the rat gastrointestinal tract decrease during fasting. Am J Physiol Endocrinol Metab 279:E815-E822.
28. Wagner J, Palfreyman M, Zraika M (1979) Determination of dopa, dopamine, dopac, epinephrine, norepinephrine, alpha-monofluoromethyldopa and alpha-difluoromethyldopa in various tissues of mice and rats using reversed-phase ion-pair liquid chromatography with electrochemical detection. J Chromatogr A 164:41-54. (Pubitemid 10230122)
29. Walker JK, Gainetdinov RR, Mangel AW, Caron MG, Shetzline MA (2000) Mice lacking the dopamine transporter display altered regulation of distal colonic motility. Am J Physiol Gastrointest Liver Physiol 279:G311-G318.
30. Winkler F, et al. (2004) Kinetics of vascular normalization by VEGFR2 blockade governs brain tumor response to radiation: Role of oxygenation, angiopoietin-1, and matrix metalloproteinases. Cancer Cell 6:553-563. (Pubitemid 40017699)
31. Satchi-Fainaro R, et al. (2005) Inhibition of vessel permeability by TNP-470 and its polymer conjugate, caplostatin. Cancer Cell 7:251-261. (Pubitemid 40568684)
32. Zaroslinski JF, et al. (1977) The pharmacology and subacute toxicology of dopamine. Proc R Soc Med 70(Suppl 2):2-6.
33. Berdel WE, et al. (1988) Influence of 1-beta-D-arabinofuranosylcytosine conjugates of lipids on the growth and metastasis of Lewis lung carcinoma. Cancer Res 48:826-829. (Pubitemid 18061871)
34. Samoszuk MK, Walter J, Mechetner E (2004) Improved immunohistochemical method for detecting hypoxia gradients in mouse tissues and tumors. J Histochem Cytochem 52:837-839. (Pubitemid 38703139)
35. Ley CD, Horsman MR, Kristjansen PE (2007) Early effects of combretastatin-A4 disodium phosphate on tumor perfusion and interstitial fluid pressure. Neoplasia 9:108-112.
36. Sarkar C, Chakroborty D, Chowdhury UR, Dasgupta PS, Basu S (2008) Dopamine increases the efficacy of anticancer drugs in breast and colon cancer preclinical models. Clin Cancer Res 14:2502-2510. (Pubitemid 351551086)
37. Adams ER, Leffert JJ, Craig DJ, Spector T, Pizzorno G (1999) In vivo effect of 5-ethynyluracil on 5-fluorouracil metabolism determined by 19F nuclear magnetic resonance spectroscopy. Cancer Res 59:122-127. (Pubitemid 29062967)
38. Remaud G, Boisdron-Celle M, Morel A, Gamelin A (2005) Sensitive MS/MS-liquid chromatography assay for simultaneous determination of tegafur, 5-fluorouracil and 5-fluorodihydrouracil in plasma. J Chromatogr B Analyt Technol Biomed Life Sci 824:153-160. (Pubitemid 41215593)
39. Armulik A, Abramsson A, Betsholtz C (2005) Endothelial/pericyte interactions. Circ Res 97:512-523. (Pubitemid 41361741)
40. Morikawa S, et al. (2002) Abnormalities in pericytes on blood vessels and endothelial sprouts in tumors. Am J Pathol 160:985-1000. (Pubitemid 34224587)
41. Bagley RG, Weber W, Rouleau C, Teicher BA (2005) Pericytes and endothelial precursor cells: Cellular interactions and contributions to malignancy. Cancer Res 65:9741-9750. (Pubitemid 41541451)
42. Jain RK (2003) Molecular regulation of vessel maturation. Nat Med 9:685-693.
43. Fiedler U, Augustin HG (2006) Angiopoietins: A link between angiogenesis and inflammation. Trends Immunol 27:552-558. (Pubitemid 44780853)
44. Lamalice L, Le Boeuf F, Huot J (2007) Endothelial cell migration during angiogenesis. Circ Res 100:782-794. (Pubitemid 46555683)
45. Ewing AG, Bigelow JC, Wightman RM (1983) Direct in vivo monitoring of dopamine released from two striatal compartments in the rat. Science 221:169-171. (Pubitemid 13063857)
46. Cai J, Kehoe O, Smith GM, Hykin P, Boulton ME (2008) The angiopoietin/Tie-2 system regulates pericyte survival and recruitment in diabetic retinopathy. Invest Ophthalmol Vis Sci 49:2163-2171.
47. Iurlaro M, et al. (2003) Rat aorta-derived mural precursor cells express the Tie2 receptor and respond directly to stimulation by angiopoietins. J Cell Sci 116:3635-3643.
48. Dekker RJ, et al. (2006) KLF2 provokes a gene expression pattern that establishes functional quiescent differentiation of the endothelium. Blood 107:4354-4363. (Pubitemid 43801361)
49. Boon RA, et al. (2007) KLF2 suppresses TGF-beta signaling in endothelium through induction of Smad7 and inhibition of AP-1. Arterioscler Thromb Vasc Biol 27:532-539.
50. Chakroborty D, et al. (2004) Depleted dopamine in gastric cancer tissues: Dopamine treatment retards growth of gastric cancer by inhibiting angiogenesis. Clin Cancer Res 10:4349-4356. (Pubitemid 38878873)
51. Lin Z, et al. (2010) Kruppel-like factor 2 regulates endothelial barrier function. Arterioscler Thromb Vasc Biol 30:1952-1959.
52. Sohn SJ, Li D, Lee LK, Winoto A (2005) Transcriptional regulation of tissue-specific genes by the ERK5 mitogen-activated protein kinase. Mol Cell Biol 25:8553-8566. (Pubitemid 41369176)
53. Roberts OL, Holmes K, Müller J, Cross DA, Cross MJ (2009) ERK5 and the regulation of endothelial cell function. Biochem Soc Trans 37:1254-1259.
54. Nigro P, et al. (2010) PKCzeta decreases eNOS protein stability via inhibitory phosphorylation of ERK5. Blood 116:1971-1979.
55. Anderson KP, Kern CB, Crable SC, Lingrel JB (1995) Isolation of a gene encoding a functional zinc finger protein homologous to erythroid Krüppel-like factor: Identification of a new multigene family. Mol Cell Biol 15:5957-5965.
56. Kuo CT, et al. (1997) The LKLF transcription factor is required for normal tunica media formation and blood vessel stabilization during murine embryogenesis. Genes Dev 11:2996-3006. (Pubitemid 27508510)
57. Jain RK, Finn AV, Kolodgie FD, Gold HK, Virmani R (2007) Antiangiogenic therapy for normalization of atherosclerotic plaque vasculature: A potential strategy for plaque stabilization. Nat Clin Pract Cardiovasc Med 4:491-502. (Pubitemid 47316647)