Chronic insulin treatment amplifies PDGF-induced motility in differentiated aortic smooth muscle cells by suppressing the expression and function of PTP1B

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 295, Issue 1, 2008, Pages

  Zhuang, Daming ^a   Pu, Qinghua ^a   Ceacareanu, Bogdan ^a,c   Chang, Yingzi ^a,b   Dixit, Madhulika ^a,d   Hassid, Aviv ^a  

^a UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^b A T STILL UNIVERSITY   (United States)

^c AT Still University ^*  (United States)

^d INDIAN INSTITUTE OF TECHNOLOGY MADRAS   (India)

Author keywords

Akt; Phosphatidylinositol 3 kinase ; Primary culture; Vascular pathology

Indexed keywords

INSULIN; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3 KINASE INHIBITOR; PLATELET DERIVED GROWTH FACTOR; PROTEIN KINASE B; PROTEIN TYROSINE PHOSPHATASE 1B; MESSENGER RNA; PLATELET DERIVED GROWTH FACTOR BB; PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR; PLATELET-DERIVED GROWTH FACTOR BB; PROTEIN KINASE INHIBITOR; PTPN1 PROTEIN, RAT; RECOMBINANT PROTEIN;

ANIMAL CELL; AORTA MEDIA; ARTICLE; CELL DIFFERENTIATION; CELL MOTILITY; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; MALE; MITOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RAT; SMOOTH MUSCLE FIBER; ANIMAL; CELL CULTURE; CELL MOTION; DRUG ANTAGONISM; DRUG EFFECT; ENZYMOLOGY; GENETICS; HUMAN; HYPERINSULINISM; METABOLISM; MUTATION; PATHOLOGY; PHOSPHORYLATION; SPRAGUE DAWLEY RAT; THORACIC AORTA; VASCULAR SMOOTH MUSCLE;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; AORTA, THORACIC; CELL DIFFERENTIATION; CELL MOVEMENT; CELLS, CULTURED; HUMANS; HYPERINSULINISM; INSULIN; MALE; MUSCLE, SMOOTH, VASCULAR; MUTATION; MYOCYTES, SMOOTH MUSCLE; PHOSPHORYLATION; PLATELET-DERIVED GROWTH FACTOR; PROTEIN KINASE INHIBITORS; PROTEIN TYROSINE PHOSPHATASE, NON-RECEPTOR TYPE 1; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, PLATELET-DERIVED GROWTH FACTOR BETA; RECOMBINANT PROTEINS; RNA, MESSENGER;

EID: 49849085888     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.01105.2007     Document Type: Article

References (63)

1. Abe J, Deguchi J, Matsumoto T, Takuwa N, Noda M, Ohno M, Makuuchi M, Kurokawa K, Takuwa Y. Stimulated activation of platelet-derived growth factor receptor in vivo in balloon-injured arteries: a link between angiotensin II and intimal thickening. Circulation 96: 1906-1913, 1997.
2. Bonora E, Tessari R, Micciolo R, Zenere M, Targher G, Padovani R, Falezza G, Muggeo M. Intimal-medial thickness of the carotid artery in nondiabetic and NIDDM patients. Relationship with insulin resistance. Diabetes Care 20: 627-631, 1997.
3. Brown C, Pan X, Hassid A. Nitric oxide and C-type atrial natriuretic peptide stimulate primary aortic smooth muscle cell migration via a cGMP-dependent mechanism: relationship to microfilament dissociation and altered cell morphology. Circ Res 84: 655-667, 1999.
4. Chang Y, Ceacareanu B, Dixit M, Sreejayan N, Hassid A. Nitric oxide-induced motility in aortic smooth muscle cells: role of protein tyrosine phosphatase SHP-2 and GTP-binding protein Rho. Circ Res 91: 390-397, 2002.
5. Chang Y, Ceacareanu B, Zhuang D, Zhang C, Pu Q, Ceacareanu AC, Hassid A. Counter-regulatory function of protein tyrosine phosphatase 1B in platelet-derived growth factor-or fibroblast growth factor-induced motility and proliferation of cultured smooth muscle cells and in neointima formation. Arterioscler Thromb Vasc Biol 26: 501-507, 2006.
6. Chang Y, Zhuang D, Zhang C, Hassid A. Increase of PTP levels in vascular injury and in cultured aortic smooth muscle cells treated with specific growth factors. Am J Physiol Heart Circ Physiol 287: H2201-H2208, 2004.
7. Cirri P, Taddei ML, Chiarugi P, Buricchi F, Caselli A, Paoli P, Giannoni E, Camici G, Manao G, Raugei G, Ramponi G. Insulin inhibits platelet-derived growth factor-induced cell proliferation. Mol Biol Cell 16: 73-83, 2005.
8. Dadke S, Kusari A, Kusari J. Phosphorylation and activation of protein tyrosine phosphatase (PTP) 1B by insulin receptor. Mol Cell Biochem 221: 147-154, 2001.
9. Dahlfors G, Chen Y, Gustafsson B, Arnqvist HJ. Inhibitory effect of diabetes on proliferation of vascular smooth muscle after balloon injury in rat aorta. Int J Exp Diabetes Res 1: 101-109, 2000.
10. Davies SP, Reddy H, Caivano M, Cohen P. Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem J 351: 95-105, 2000.
11. De Pergola G, Ciccone M, Pannacciulli N, Modugno M, Sciaraffia M, Minenna A, Rizzon P, Giorgino R. Lower insulin sensitivity as an independent risk factor for carotid wall thickening in normotensive, non-diabetic, non-smoking normal weight and obese premenopausal women. Int J Obes Relat Metab Disord 24: 825-829, 2000.
12. Dixit M, Zhuang D, Ceacareanu B, Hassid A. Treatment with insulin uncovers the motogenic capacity of nitric oxide in aortic smooth muscle cells: dependence on Gab1 and Gab1-SHP2 association. Circ Res 93: e113-123, 2003.
13. Englesbe MJ, Davies MG, Hawkins SM, Hsieh PC, Daum G, Kenagy RD, Clowes AW. Arterial injury repair in nonhuman primates-the role of PDGF receptor-beta. J Surg Res 119: 80-84, 2004.
14. Faber JE, Yang N. Balloon injury alters alpha-adrenoceptor expression across rat carotid artery wall. Clin Exp Pharmacol Physiol 33: 204-210, 2006.
15. Ferns GA, Raines EW, Sprugel KH, Motani AS, Reidy MA, Ross R. Inhibition of neointimal smooth muscle accumulation after angioplasty by an antibody to PDGF. Science 253: 1129-1132, 1991.
16. Fishbein I, Waltenberger J, Banai S, Rabinovich L, Chorny M, Levitzki A, Gazit A, Huber R, Mayr U, Gertz SD, Golomb G. Local delivery of platelet-derived growth factor receptor-specific tyrphostin inhibits neointimal formation in rats. Arterioscler Thromb Vasc Biol 20: 667-676, 2000.
17. Flint AJ, Tiganis T, Barford D, Tonks NK. Development of "substratetrapping" mutants to identify physiological substrates of protein tyrosine phosphatases. Proc Natl Acad Sci USA 94: 1680-1685, 1997.
18. Giese NA, Marijianowski MM, McCook O, Hancock A, Ramakrishnan V, Fretto LJ, Chen C, Kelly AB, Koziol JA, Wilcox JN, Hanson SR. The role of alpha and beta platelet-derived growth factor receptor in the vascular response to injury in nonhuman primates. Arterioscler Thromb Vasc Biol 19: 900-909, 1999.
19. Goalstone ML, Natarajan R, Standley PR, Walsh MF, Leitner JW, Carel K, Scott S, Nadler J, Sowers JR, Draznin B. Insulin potentiates platelet-derived growth factor action in vascular smooth muscle cells. Endocrinology 139: 4067-4072, 1998.
20. Haj FG, Markova B, Klaman LD, Bohmer FD, Neel BG. Regulation of receptor tyrosine kinase signaling by protein tyrosine phosphatase-1B. J Biol Chem 278: 739-744, 2003.
21. Hart CE, Kraiss LW, Vergel S, Gilbertson D, Kenagy R, Kirkman T, Crandall DL, Tickle S, Finney H, Yarranton G, Clowes AW. PDGF-beta receptor blockade inhibits intimal hyperplasia in the baboon. Circulation 99: 564-569, 1999.
22. Hassid A, Arabshahi H, Bourcier T, Dhaunsi GS, Matthews C. Nitric oxide selectively amplifies FGF-2-induced mitogenesis in primary rat aortic smooth muscle cells. Am J Physiol Heart Circ Physiol 267: H1040-H1048, 1994.
23. Hassid A, Yao J, Huang S. NO alters cell shape and motility in aortic smooth muscle cells via protein tyrosine phosphatase 1B activation. Am J Physiol Heart Circ Physiol 277: H1014-H1026, 1999.
24. Heldin CH, Ostman A, Ronnstrand L. Signal transduction via platelet-derived growth factor receptors. Biochim Biophys Acta 1378: F79-113, 1998.
25. Imai Y, Clemmons DR. Roles of phosphatidylinositol 3-kinase and mitogen-activated protein kinase pathways in stimulation of vascular smooth muscle cell migration and deoxyribonucleic acid synthesis by insulin-like growth factor-I. Endocrinology 140: 4228-4235, 1999.
26. Indolfi C, Torella D, Cavuto L, Davalli AM, Coppola C, Esposito G, Carriero MV, Rapacciuolo A, Di Lorenzo E, Stabile E, Perrino C, Chieffo A, Pardo F, Chiariello M. Effects of balloon injury on neointimal hyperplasia in streptozotocin-induced diabetes and in hyperinsulinemic nondiabetic pancreatic islet-transplanted rats. Circulation 103: 2980-2986, 2001.
27. Jacob A, Molkentin JD, Smolenski A, Lohmann SM, Begum N. Insulin inhibits PDGF-directed VSMC migration via NO/cGMP increase of MKP-1 and its inactivation of MAPKs. Am J Physiol Cell Physiol 283: C704-C713, 2002.
28. Jawien A, Bowen-Pope DF, Lindner V, Schwartz SM, Clowes AW. Platelet-derived growth factor promotes smooth muscle migration and intimal thickening in a rat model of balloon angioplasty. J Clin Invest 89: 507-511, 1992.
29. Kahn AM, Allen JC, Seidel CL, Zhang S. Insulin inhibits migration of vascular smooth muscle cells with inducible nitric oxide synthase. Hypertension 35: 303-306, 2000.
30. Kobayashi T, Hayashi Y, Taguchi K, Matsumoto T, Kamata K. ANG II enhances contractile responses via PI3-kinase p110-δ pathway in aortas from diabetic rats with systemic hyperinsulinemia. Am J Physiol Heart Circ Physiol 291: H846-H853, 2006.
31. Kong M, Mounier C, Wu J, Posner BI. Epidermal growth factorinduced phosphatidylinositol 3-kinase activation and DNA synthesis. Identification of Grb2-associated binder 2 as the major mediator in rat hepatocytes. J Biol Chem 275: 36035-36042, 2000.
32. Kornowski R, Mintz GS, Kent KM, Pichard AD, Satler LF, Bucher TA, Hong MK, Popma JJ, Leon MB. Increased restenosis in diabetes mellitus after coronary interventions is due to exaggerated intimal hyperplasia. A serial intravascular ultrasound study. Circulation 95: 1366-1369, 1997.
33. Kundra V, Escobedo JA, Kazlauskas A, Kim HK, Rhee SG, Williams LT, Zetter BR. Regulation of chemotaxis by the platelet-derived growth factor receptor-beta. Nature 367: 474-476, 1994.
34. Levitzki A. PDGF receptor kinase inhibitors for the treatment of restenosis. Cardiovasc Res 65: 581-586, 2005.
35. Li C, Ford ES, McGuire LC, Mokdad AH, Little RR, Reaven GM. Trends in hyperinsulinemia among nondiabetic adults in the U.S. Diabetes Care 29: 2396-2402, 2006.
36. Mahadev K, Zilbering A, Zhu L, Goldstein BJ. Insulin-stimulated hydrogen peroxide reversibly inhibits protein-tyrosine phosphatase 1b in vivo and enhances the early insulin action cascade. J Biol Chem 276: 21938-21942, 2001.
37. Meng TC, Buckley DA, Galic S, Tiganis T, Tonks NK. Regulation of insulin signaling through reversible oxidation of the protein-tyrosine phosphatases TC45 and PTP1B. J Biol Chem 279: 37716-37725, 2004.
38. Myllarniemi M, Calderon L, Lemstrom K, Buchdunger E, Hayry P. Inhibition of platelet-derived growth factor receptor tyrosine kinase inhibits vascular smooth muscle cell migration and proliferation. FASEB J 11: 1119-1126, 1997.
39. Noiseux N, Boucher CH, Cartier R, Sirois MG. Bolus endovascular PDGFR-beta antisense treatment suppressed intimal hyperplasia in a rat carotid injury model. Circulation 102: 1330-1336, 2000.
40. Ogihara T, Asano T, Ando K, Chiba Y, Sakoda H, Anai M, Shojima N, Ono H, Onishi Y, Fujishiro M, Katagiri H, Fukushima Y, Kikuchi M, Noguchi N, Aburatani H, Komuro I, Fujita T. Angiotensin II-induced insulin resistance is associated with enhanced insulin signaling. Hypertension 40: 872-879, 2002.
41. Ogihara T, Asano T, Ando K, Chiba Y, Sekine N, Sakoda H, Anai M, Onishi Y, Fujishiro M, Ono H, Shojima N, Inukai K, Fukushima Y, Kikuchi M, Fujita T. Insulin resistance with enhanced insulin signaling in high-salt diet-fed rats. Diabetes 50: 573-583, 2001.
42. Onishi Y, Honda M, Ogihara T, Sakoda H, Anai M, Fujishiro M, Ono H, Shojima N, Fukushima Y, Inukai K, Katagiri H, Kikuchi M, Oka Y, Asano T. Ethanol feeding induces insulin resistance with enhanced PI 3-kinase activation. Biochem Biophys Res Commun 303: 788-794, 2003.
43. Pagliassotti MJ, Kang J, Thresher JS, Sung CK, Bizeau ME. Elevated basal PI 3-kinase activity and reduced insulin signaling in sucrose-induced hepatic insulin resistance. Am J Physiol Endocrinol Metab 282: E170-E176, 2002.
44. Panek RL, Dahring TK, Olszewski BJ, Keiser JA. PDGF receptor protein tyrosine kinase expression in the balloon-injured rat carotid artery. Arterioscler Thromb Vasc Biol 17: 1283-1288, 1997.
45. Park SH, Marso SP, Zhou Z, Foroudi F, Topol EJ, Lincoff AM. Neointimal hyperplasia after arterial injury is increased in a rat model of non-insulin-dependent diabetes mellitus. Circulation 104: 815-819, 2001.
46. Ravichandran LV, Chen H, Li Y, Quon MJ. Phosphorylation of PTP1B at Ser(50) by Akt impairs its ability to dephosphorylate the insulin receptor. Mol Endocrinol 15: 1768-1780, 2001.
47. Sano H, Sudo T, Yokode M, Murayama T, Kataoka H, Takakura N, Nishikawa S, Nishikawa SI, Kita T. Functional blockade of platelet-derived growth factor receptor-beta but not of receptor-alpha prevents vascular smooth muscle cell accumulation in fibrous cap lesions in apolipoprotein E-deficient mice. Circulation 103: 2955-2960, 2001.
48. Shepherd PR. Mechanisms regulating phosphoinositide 3-kinase signalling in insulin-sensitive tissues. Acta Physiol Scand 183: 3-12, 2005.
49. Sirois MG, Simons M, Edelman ER. Antisense oligonucleotide inhibition of PDGFR-beta receptor subunit expression directs suppression of intimal thickening. Circulation 95: 669-676, 1997.
50. Sreejayan N, Lin Y, Hassid A. NO attenuates insulin signaling and motility in aortic smooth muscle cells via protein tyrosine phosphatase 1B-mediated mechanism. Arterioscler Thromb Vasc Biol 22: 1086-1092, 2002.
51. Suzuki LA, Poot M, Gerrity RG, Bornfeldt KE. Diabetes accelerates smooth muscle accumulation in lesions of atherosclerosis: lack of direct growth-promoting effects of high glucose levels. Diabetes 50: 851-860, 2001.
52. Takagi T, Yoshida K, Akasaka T, Kaji S, Kawamoto T, Honda Y, Yamamuro A, Hozumi T, Morioka S. Hyperinsulinemia during oral glucose tolerance test is associated with increased neointimal tissue proliferation after coronary stent implantation in nondiabetic patients: a serial intravascular ultrasound study. J Am Coll Cardiol 36: 731-738, 2000.
53. Tao J, Malbon CC, Wang HY. Insulin stimulates tyrosine phosphorylation and inactivation of protein-tyrosine phosphatase 1B in vivo. J Biol Chem 276: 29520-29525, 2001.
54. Taylor AM, Hanchett R, Natarajan R, Hedrick CC, Forrest S, Nadler JL, McNamara CA. The effects of leukocyte-type 12/15-lipoxygenase on Id3-mediated vascular smooth muscle cell growth. Arterioscler Thromb Vasc Biol 25: 2069-2074, 2005.
55. Toba H, Gomyo E, Miki S, Shimizu T, Yoshimura A, Inoue R, Sawai N, Tsukamoto R, Asayama J, Kobara M, Nakata T. Hyperinsulinaemia increases the gene expression of endothelial nitric oxide synthase and the phosphatidylinositol 3-kinase/akt pathway in rat aorta. Clin Exp Pharmacol Physiol 33: 440-447, 2006.
56. Wang PW, Liou CW, Wang ST, Eng HL, Liu RT, Tung SC, Chien WY, Lu YC, Kuo MC, Hsieh CJ, Chen CH, Chen JF, Chu JW, Reaven GM. Relative impact of low-density lipoprotein-cholesterol concentration and insulin resistance on carotid wall thickening in nondiabetic, normotensive volunteers. Metabolism 51: 255-259, 2002.
57. Watson KE, Peters Harmel AL, Matson G. Atherosclerosis in type 2 diabetes mellitus: the role of insulin resistance. J Cardiovasc Pharmacol Ther 8: 253-260, 2003.
58. Wilcox JN, Smith KM, Williams LT, Schwartz SM, Gordon D. Platelet-derived growth factor mRNA detection in human atherosclerotic plaques by in situ hybridization. J Clin Invest 82: 1134-1143, 1988.
59. Yamada H, Tsushima T, Murakami H, Uchigata Y, Iwamoto Y. Potentiation of mitogenic activity of platelet-derived growth factor by physiological concentrations of insulin via the MAP kinase cascade in rat A10 vascular smooth muscle cells. Int J Exp Diabetes Res 3: 131-144, 2002.
60. Yamasaki Y, Miyoshi K, Oda N, Watanabe M, Miyake H, Chan J, Wang X, Sun L, Tang C, McMahon G, Lipson KE. Weekly dosing with the platelet-derived growth factor receptor tyrosine kinase inhibitor SU9518 significantly inhibits arterial stenosis. Circ Res 88: 630-636, 2001.
61. Yamasaki Y, Miyoshi K, Oda N, Watanabe M, Miyake H, Chan J, Wang X, Sun L, Tang C, McMahon G, Lipson KE. Weekly dosing with the platelet-derived growth factor receptor tyrosine kinase inhibitor SU9518 significantly inhibits arterial stenosis. Circ Res 88: 630-636, 2001.
62. Zavaroni I, Ardigo D, Zuccarelli A, Pacetti E, Piatti PM, Monti L, Valtuena S, Massironi P, Rossi PC, Reaven GM. Insulin resistance/ compensatory hyperinsulinemia predict carotid intimal medial thickness in patients with essential hypertension. Nutr Metab Cardiovasc Dis 16: 22-27, 2006.
63. Zhuang D, Ceacareanu AC, Lin Y, Ceacareanu B, Dixit M, Chapman KE, Waters CM, Rao GN, Hassid A. Nitric oxide attenuates insulin- or IGF-I-stimulated aortic smooth muscle cell motility by decreasing H2O2 levels: essential role of cGMP. Am J Physiol Heart Circ Physiol 286: H2103-H2112, 2004.