Contributions of VEGF to age-dependent transmural gradients in contractile protein expression in ovine carotid arteries

American Journal of Physiology - Cell Physiology

Volumn 301, Issue 3, 2011, Pages

  Butler, Stacy M ^a   Abrassart, Jenna M ^a   Hubbell, Margaret C ^a   Adeoye, Olayemi ^a   Semotiuk, Andrew ^a   Williams, James M ^a   Mata Greenwood, Eugenia ^a   Khorram, Omid ^a   Pearce, William J ^a  

^a LOMA LINDA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Myosin light chain kinase; Organ culture; Regulatory myosin light chain; Smooth muscle; Vascular endothelial growth factor receptors

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; CONTRACTILE PROTEIN; MESSENGER RNA; MYOSIN LIGHT CHAIN KINASE; POTASSIUM; VASCULOTROPIN; VASCULOTROPIN A; VASCULOTROPIN RECEPTOR 1; VASCULOTROPIN RECEPTOR 2;

ADVENTITIA; AGE; ANIMAL TISSUE; ARTERY MUSCLE; ARTERY WALL; ARTICLE; CAROTID ARTERY; CONTROLLED STUDY; FEMALE; FETUS; IMMUNOHISTOCHEMISTRY; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; ORGAN CULTURE; PHENOTYPE; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; SMOOTH MUSCLE CONTRACTILITY; SMOOTH MUSCLE FIBER; STRESS STRAIN RELATIONSHIP; TRANSMURAL GRADIENT; VASCULAR ENDOTHELIUM;

ACTINS; AGING; ANIMALS; CAROTID ARTERY, COMMON; CONTRACTILE PROTEINS; CULTURE MEDIA, SERUM-FREE; FEMALE; FETUS; GENE EXPRESSION; MALE; MUSCLE CONTRACTION; MUSCLE, SMOOTH, VASCULAR; MYOSIN LIGHT CHAINS; MYOSIN-LIGHT-CHAIN KINASE; NITRIC OXIDE SYNTHASE TYPE III; ORGAN CULTURE TECHNIQUES; POTASSIUM; SHEEP; STRESS, MECHANICAL; TUNICA MEDIA; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-1; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

BOVINAE; OVIS;

EID: 80052220417     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00413.2010     Document Type: Article

References (65)

1. Abraham NG, Scapagnini G, Kappas A. Human heme oxygenase: cell cycle-dependent expression and DNA microarray identification of multiple gene responses after transduction of endothelial cells. J Cell Biochem 90: 1098-1111, 2003.
2. Alon T, Hemo I, Itin A, Pe'er J, Stone J, Keshet E. Vascular endothelial growth factor acts as a survival factor for newly formed retinal vessels and has implications for retinopathy of prematurity. Nat Med 1: 1024-1028, 1995.
3. Bagnard D, Vaillant C, Khuth ST, Dufay N, Lohrum M, Puschel AW, Belin MF, Bolz J, Thomasset N. Semaphorin 3A-vascular endothelial growth factor-165 balance mediates migration and apoptosis of neural progenitor cells by the recruitment of shared receptor. J Neurosci 21: 3332-3341, 2001.
4. Ball SG, Shuttleworth CA, Kielty CM. Vascular endothelial growth factor can signal through platelet-derived growth factor receptors. J Cell Biol 177: 489-500, 2007.
5. Balligand JL, Feron O, Dessy C. eNOS activation by physical forces: from short-term regulation of contraction to chronic remodeling of cardiovascular tissues. Physiol Rev 89: 481-534, 2009.
6. Barrientos S, Stojadinovic O, Golinko MS, Brem H, Tomic-Canic M. Growth factors and cytokines in wound healing. Wound Repair Regen 16: 585-601, 2008.
7. Bausero P, Ben-Mahdi M, Mazucatelli J, Bloy C, Perrot-Applanat M. Vascular endothelial growth factor is modulated in vascular muscle cells by estradiol, tamoxifen, and hypoxia. Am J Physiol Heart Circ Physiol 279: H2033-H2042, 2000.
8. Bevan RD. Effect of sympathetic denervation on smooth muscle cell proliferation in the growing rabbit ear artery. Circ Res 37: 14-19, 1975.
9. Bryan BA, Walshe TE, Mitchell DC, Havumaki JS, Saint-Geniez M, Maharaj AS, Maldonado AE, D'Amore PA. Coordinated vascular endothelial growth factor expression and signaling during skeletal myogenic differentiation. Mol Biol Cell 19: 994-1006, 2008.
10. Chandra A, Angle N. Vascular endothelial growth factor stimulates a novel calcium-signaling pathway in vascular smooth muscle cells. Surgery 138: 780-787, 2005.
11. 2+ sensitization in age-dependent cerebrovascular myogenic tone. Am J Physiol Heart Circ Physiol 299: H1034-H1044, 2010.
12. Connolly DT, Heuvelman DM, Nelson R, Olander JV, Eppley BL, Delfino JJ, Siegel NR, Leimgruber RM, Feder J. Tumor vascular permeability factor stimulates endothelial cell growth and angiogenesis. J Clin Invest 84: 1470-1478, 1989.
13. Dao HH, Bouvet C, Moreau S, Beaucage P, Lariviere R, Servant MJ, de Champlain J, Moreau P. Endothelin is a dose-dependent trophic factor and a mitogen in small arteries in vivo. Cardiovasc Res 71: 61-68, 2006.
14. Davis MJ, Hill MA. Signaling mechanisms underlying the vascular myogenic response. Physiol Rev 79: 387-423, 1999.
15. de Araujo LF, Grozovsky R, dos Santos Pereira MJ, de Carvalho JJ, Vaisman M, Carvalho DP. Expressions of vascular endothelial growth factor and nitric oxide synthase III in the thyroid gland of ovariectomized rats are upregulated by estrogen and selective estrogen receptor modulators. Thyroid 20: 85-92, 2010.
16. Dvorak HF, Brown LF, Detmar M, Dvorak AM. Vascular permeability factor/vascular endothelial growth factor, microvascular hyperpermeability, and angiogenesis. Am J Pathol 146: 1029-1039, 1995.
17. Dvorak HF, Dvorak AM, Manseau EJ, Wiberg L, Churchill WH. Fibrin gel investment associated with line 1 and line 10 solid tumor growth, angiogenesis, and fibroplasia in guinea pigs. Role of cellular immunity, myofibroblasts, microvascular damage, and infarction in line 1 tumor regression. J Natl Cancer Inst 62: 1459-1472, 1979.
18. Elliott CF, Pearce WJ. Effects of maturation on cell water, protein, and DNA content in ovine cerebral arteries. J Appl Physiol 79: 831-837, 1995.
19. Freitas-Andrade M, Carmeliet P, Stanimirovic DB, Moreno M. VEGFR-2-mediated increased proliferation and survival in response to oxygen and glucose deprivation in PlGF knockout astrocytes. J Neurochem 107: 756-767, 2008.
20. Frid MG, Moiseeva EP, Stenmark KR. Multiple phenotypically distinct smooth muscle cell populations exist in the adult and developing bovine pulmonary arterial media in vivo. Circ Res 75: 669-681, 1994.
21. Giuriato L, Scatena M, Chiavegato A, Tonello M, Scannapieco G, Pauletto P, Sartore S. Nonmuscle myosin isoforms and cell heterogeneity in developing rabbit vascular smooth muscle. J Cell Sci 101: 233-246, 1992.
22. Grosskreutz CL, Anand-Apte B, Duplaa C, Quinn TP, Terman BI, Zetter B, D'Amore PA. Vascular endothelial growth factor-induced migration of vascular smooth muscle cells in vitro. Microvasc Res 58: 128-136, 1999.
23. Gustincich S, Schneider C. Serum deprivation response gene is induced by serum starvation but not by contact inhibition. Cell Growth Differ 4: 753-760, 1993.
24. Hermann DM, Zechariah A. Implications of vascular endothelial growth factor for postischemic neurovascular remodeling. J Cereb Blood Flow Metab 29: 1620-1643, 2009.
25. Hoeben A, Landuyt B, Highley MS, Wildiers H, Van Oosterom AT, De Bruijn EA. Vascular endothelial growth factor and angiogenesis. Pharmacol Rev 56: 549-580, 2004.
26. Holifield B, Helgason T, Jemelka S, Taylor A, Navran S, Allen J, Seidel C. Differentiated vascular myocytes: are they involved in neointimal formation? J Clin Invest 97: 814-825, 1996.
27. Hull A, Long D, Longo L, Pearce W. Pregnancy-induced changes in ovine cerebral arteries. Am J Physiol Regul Integr Comp Physiol 262: R137-R143, 1992.
28. Injeti ER, Sandoval RJ, Williams JM, Smolensky AV, Ford LE, Pearce WJ. Maximal stimulation-induced in situ myosin light chain kinase activity is upregulated in fetal compared with adult ovine carotid arteries. Am J Physiol Heart Circ Physiol 295: H2289-H2298, 2008.
29. Ishida A, Murray J, Saito Y, Kanthou C, Benzakour O, Shibuya M, Wijelath ES. Expression of vascular endothelial growth factor receptors in smooth muscle cells. J Cell Physiol 188: 359-368, 2001.
30. Jin KL, Mao XO, Greenberg DA. Vascular endothelial growth factor: direct neuroprotective effect in in vitro ischemia. Proc Natl Acad Sci USA 97: 10242-10247, 2000.
31. Jin X, Ge X, Zhu DL, Yan C, Chu YF, Chen WD, Liu J, Gao PJ. Expression and function of vascular endothelial growth factor receptors (Flt-1 and Flk-1) in vascular adventitial fibroblasts. J Mol Cell Cardiol 43: 292-300, 2007.
32. Kato M, Kyogoku M. Competence growth factors evoke the phenotypic transition of arterial smooth muscle cells. Ann NY Acad Sci 598: 232-237, 1990.
33. Kermani P, Hempstead B. Brain-derived neurotrophic factor: a newly described mediator of angiogenesis. Trends Cardiovasc Med 17: 140-143, 2007.
34. Leung DW, Cachianes G, Kuang WJ, Goeddel DV, Ferrara N. Vascular endothelial growth factor is a secreted angiogenic mitogen. Science 246: 1306-1309, 1989.
35. Li D, Zhang C, Song F, Lubenec I, Tian Y, Song QH. VEGF regulates FGF-2 and TGF-beta1 expression in injury endothelial cells and mediates smooth muscle cells proliferation and migration. Microvasc Res 77: 134-142, 2008.
36. Liu Y, Cox SR, Morita T, Kourembanas S. Hypoxia regulates vascular endothelial growth factor gene expression in endothelial cells. Identification of a 5= enhancer. Circ Res 77: 638-643, 1995.
37. MacDougall JD, Biswas S, Cook RP. The effects of certain C27 steroids on organ cultures of rabbit aorta. Br J Exp Pathol 46: 549-553, 1965.
38. Manoury B, Etheridge SL, Reid J, Gurney AM. Organ culture mimics the effects of hypoxia on membrane potential, K(+) channels and vessel tone in pulmonary artery. Br J Pharmacol 158: 848-861, 2009.
39. Marko SB, Damon DH. VEGF promotes vascular sympathetic innervation. Am J Physiol Heart Circ Physiol 294: H2646-H2652, 2008.
40. Miller JW. Vascular endothelial growth factor and ocular neovascularization. Am J Pathol 151: 13-23, 1997.
41. Nauli SM, Williams JM, Gerthoffer WT, Pearce WJ. Chronic hypoxia modulates relations among calcium, myosin light chain phosphorylation, and force differently in fetal and adult ovine basilar arteries. J Appl Physiol 99: 120-127, 2005.
42. Nilsson I, Shibuya M, Wennstrom S. Differential activation of vascular genes by hypoxia in primary endothelial cells. Exp Cell Res 299: 476-485, 2004.
43. Oishi K, Kobayashi A, Fujii K, Kanehira D, Ito Y, Uchida MK. Angiogenesis in vitro: vascular tube formation from the differentiation of neural stem cells. J Pharm Sci 96: 208-218, 2004.
44. Olfert IM, Breen EC, Mathieu-Costello O, Wagner PD. Chronic hypoxia attenuates resting and exercise-induced VEGF, flt-1, and flk-1 mRNA levels in skeletal muscle. J Appl Physiol 90: 1532-1538, 2001.
45. Osada-Oka M, Ikeda T, Imaoka S, Akiba S, Sato T. VEGF-enhanced proliferation under hypoxia by an autocrine mechanism in human vascular smooth muscle cells. J Atheroscler Thromb 15: 26-33, 2008.
46. Osol G, Laher I, Kelley M. Myogenic tone is coupled to phospholipase C and G protein activation in small cerebral arteries. Am J Physiol Heart Circ Physiol 265: H415-H420, 1993.
47. Owens GK, Kumar MS, Wamhoff BR. Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol Rev 84: 767-801, 2004.
48. Owens GK, Thompson MM. Developmental changes in isoactin expression in rat aortic smooth muscle cells in vivo. Relationship between growth and cytodifferentiation. J Biol Chem 261: 13373-13380, 1986.
49. Pearce WJ, Hull AD, Long DM, Longo LD. Developmental changes in ovine cerebral artery composition and reactivity. Am J Physiol Regul Integr Comp Physiol 261: R458-R465, 1991.
50. Peters KG, De Vries C, Williams LT. Vascular endothelial growth factor receptor expression during embryogenesis and tissue repair suggests a role in endothelial differentiation and blood vessel growth. Proc Natl Acad Sci USA 90: 8915-8919, 1993.
51. Sandoval RJ, Injeti ER, Williams JM, Georthoffer WT, Pearce WJ. Myogenic contractility is more dependent on myofilament calcium sensitization in term fetal than adult ovine cerebral arteries. Am J Physiol Heart Circ Physiol 293: H548-H556, 2007.
52. 2+ sensitivity regulation in promoting myogenic vasoconstriction. Cardiovasc Res 77: 8-18, 2008.
53. Senger DR, Galli SJ, Dvorak AM, Perruzzi CA, Harvey VS, Dvorak HF. Tumor cells secrete a vascular permeability factor that promotes accumulation of ascites fluid. Science 219: 983-985, 1983.
54. Senger DR, Van de Water L, Brown LF, Nagy JA, Yeo KT, Yeo TK, Berse B, Jackman RW, Dvorak AM, Dvorak HF. Vascular permeability factor (VPF, VEGF) in tumor biology. Cancer Metastasis Rev 12: 303-324, 1993.
55. Sondell M, Lundborg G, Kanje M. Vascular endothelial growth factor has neurotrophic activity and stimulates axonal outgrowth, enhancing cell survival and Schwann cell proliferation in the peripheral nervous system. J Neurosci 19: 5731-5740, 1999.
56. Tai K, Vandenberg G, Hamaide MC, Wibo M, Morel N. Effect of organ culture on noradrenaline-evoked contraction, calcium signalling and TRPC expression in rat mesenteric artery. J Vasc Res 46: 353-364, 2009.
57. Thorne GD, Paul RJ. Effects of organ culture on arterial gene expression and hypoxic relaxation: role of the ryanodine receptor. Am J Physiol Cell Physiol 284: C999-C1005, 2003.
58. Todd ME, Gowen B. Arterial wall and smooth muscle cell development in young Wistar rats and the effects of surgical denervation. Circ Res 69: 438-446, 1991.
59. Tsoi SC, Wen Y, Chung JY, Chen D, Magness RR, Zheng J. Coexpression of vascular endothelial growth factor and neuropilin-1 in ovine feto-placental artery endothelial cells. Mol Cell Endocrinol 196: 95-106, 2002.
60. Vonnahme KA, Wilson ME, Li Y, Rupnow HL, Phernetton TM, Ford SP, Magness RR. Circulating levels of nitric oxide and vascular endothelial growth factor throughout ovine pregnancy. J Physiol 565: 101-109, 2005.
61. Williams JM, White CR, Chang MM, Injeti ER, Zhang L, Pearce WJ. Chronic hypoxic decreases in soluble guanylate cyclase protein and enzyme activity are age dependent in fetal and adult ovine carotid arteries. J Appl Physiol 100: 1857-1866, 2006.
62. Yamawaki H, Sato K, Hori M, Ozaki H, Nakamura S, Nakayama H, Doi K, Karaki H. Morphological and functional changes of rabbit mesenteric artery cultured with fetal bovine serum. Life Sci 67: 807-820, 2000.
63. Zar JH. Biostatistical Analysis. Upper Saddle River, NJ: Prentice Hall, 1999.
64. Zetterberg A, Larsson O. Kinetic analysis of regulatory events in G1 leading to proliferation or quiescence of Swiss 3T3 cells. Proc Natl Acad Sci USA 82: 5365-5369, 1985.
65. Ziche M, Morbidelli L, Choudhuri R, Zhang HT, Donnini S, Granger HJ, Bicknell R. Nitric oxide synthase lies downstream from vascular endothelial growth factor-induced but not basic fibroblast growth factorinduced angiogenesis. J Clin Invest 99: 2625-2634, 1997.