Transgenic overexpression of pregnancy-associated plasma protein-A in murine arterial smooth muscle accelerates atherosclerotic lesion development

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 299, Issue 2, 2010, Pages

  Conover, Cheryl A ^a   Mason, Megan A ^a   Bale, Laurie K ^a   Harrington, Sean C ^a   Nyegaard, Mette ^b   Oxvig, Claus ^b   Overgaard, Michael T ^c  

^a MAYO CLINIC   (United States)

^b AARHUS UNIVERSITY   (Denmark)

^c AALBORG UNIVERSITY   (Denmark)

Author keywords

Atherosclerosis

Indexed keywords

APOLIPOPROTEIN E; CHOLESTEROL; PREGNANCY ASSOCIATED PLASMA PROTEIN A; SOMATOMEDIN BINDING PROTEIN 4; SOMATOMEDIN C;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTERY MUSCLE; ARTICLE; ATHEROSCLEROSIS; CONTROLLED STUDY; FEMALE; GENE OVEREXPRESSION; KNOCKOUT MOUSE; MACROPHAGE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TISSUE SPECIFICITY; TRANSGENIC MOUSE; WEIGHT GAIN;

ANIMALS; AORTA; APOLIPOPROTEINS E; ATHEROSCLEROSIS; CELLS, CULTURED; DISEASE MODELS, ANIMAL; FEMALE; GENOTYPE; HUMANS; INSULIN-LIKE GROWTH FACTOR BINDING PROTEIN 4; INSULIN-LIKE GROWTH FACTOR BINDING PROTEIN 5; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MICROFILAMENT PROTEINS; MUSCLE PROTEINS; MUSCLE, SMOOTH, VASCULAR; PHENOTYPE; PHOSPHORYLATION; PREGNANCY-ASSOCIATED PLASMA PROTEIN-A; PROMOTER REGIONS, GENETIC; PROTO-ONCOGENE PROTEINS C-AKT; RNA, MESSENGER; UP-REGULATION;

EID: 77955463896     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00904.2009     Document Type: Article

References (51)

1. Adamo ML, Ma X, Ackert-Bicknell CL, Donahue LR, Beamer WG, Rosen CJ. Genetic increase in serum insulin-like growth factor-I (IGF-I) in C3H/HeJ compared with C57BL/6J mice is associated with increased transcription from the IGF-I exon 2 promoter. Endocrinology 147: 2944-2955, 2006. (Pubitemid 43764630)
2. Apple FS, Wu AHB, Mair J, Ravkilde J, Panteghini M, Tate J, Pagani F, Christenson RH, Mockel M, Danne O, Jaffe AS, Committee on Standardization of Markers of Cardiac Damage of the IFCC. Future biomarkers for detection of ischemia and risk stratification in acute coronary syndrome. Clin Chem 51: 810-824, 2005.
3. Bayes-Genis A, Conover CA, Overgaard MT, Bailey KR, Christiansen M, Holmes DR Jr, Virmani R, Oxvig C, Schwartz RS. Pregnancy-associated plasma protein A as a marker of acute coronary syndromes. N Engl J Med 345: 1022-1029, 2001.
4. Bayes-Genis A, Conover Schwartz RS CA. The insulin-like growth factor axis: a review of atherosclerosis and restenosis. Circ Res 86: 125-130, 2000. (Pubitemid 30086171)
5. Bayes-Genis A, Schwartz RS, Lewis DA, Overgaard MT, Christiansen M, Oxvig C, Ashai K, Holmes DR Jr, Conover CA. Insulin-like growth factor binding protein-4 protease produced by smooth muscle cells increases in the coronary artery after angioplasty. Arterioscler Thromb Vasc Biol 21: 335-341, 2001. (Pubitemid 32199113)
6. Bennett MR, Evan GI, Schwartz SM. Apoptosis of human vascular smooth muscle cells derived from normal vessels and coronary atherosclerotic plaques. J Clin Invest 95: 2266-2274, 1995.
7. Boldt HB, Conover CA. Pregnancy-associated plasma protein-A (PAPPA): a local regulator of IGF bioavailability through cleavage of IGFBPs. Growth Horm IGF Res 17: 10-18, 2007. (Pubitemid 46299994)
8. Byun D, Mohan S, Yoo M, Sexton C, Baylink DJ, Qin X. Pregnancy-associated plasma protein-A accounts for the insulin-like growth factor (IGF)-binding protein-4 (IGFBP-4) proteolytic activity in human pregnancy serum and enhances the mitogenic activity of IGF by degrading IGFBP-4 in vitro. J Clin Endocrinol Metab 86: 847-854, 2001. (Pubitemid 32207505)
9. Clemmons DR. Modifying IGF1 activity: an approach to treat endocrine disorders, atherosclerosis and cancer. Nat Rev 6: 821-833, 2007.
10. Conover CA, Bale LK, Durham SK, Powell DR. Insulin-like growth factor (IGF) binding protein-3 potentiation of IGF action is mediated through the phosphatidylinositol-3-kinase pathway and is associated with alteration in protein kinae B/Akt sensitivity. Endocrinology 141: 3098-3103, 2000.
11. Conover CA, Bale LK, Harrington SC, Resch ZT, Overgaard MT, Oxvig C. Cytokine stimulation of pregnancy associated plasma protein A expression in human coronary artery smooth muscle cells: inhibition by resveratrol. Am J Physiol Cell Physiol 290: C183-C188, 2006.
12. Conover CA, Clarkson JT, Bale LK. Effect of glucocorticoid on insulin-like growth factor (IGF) regulation of IGF-binding protein expression in fibroblasts. Endocrinology 136: 1403-1410, 1995.
13. Conover CA, Harrington SC, Bale LK. Differential regulation of pregnancy associated plasma protein-A in human coronary artery endothelial cells and smooth muscle cells. Growth Horm IGF Res 18: 213-220, 2008.
14. Conover CA, Harrington SC, Bale LK, Oxvig C. Surface association of pregnancy associated plasma protein-A accounts for its colocalization with activated macrophages. Am J Physiol Heart Circ Physiol 292: H994-H1000, 2007. (Pubitemid 46251329)
15. Consuegra-Sanchez L, Fredericks S, Kaski JC. Pregnancy-associated plasma protein-A (PAPP-A) and cardiovascular risk. Atherosclerosis 203: 346-352, 2009.
16. Conti E, Carrozza C, Capoluongo E, Volpe M, Crea F, Zuppi C, Andreotti F. Insulin-like growth factor-1 as a vascular protective factor. Circulation 110: 2260-2265, 2004. (Pubitemid 39372511)
17. Dansky HM, Charlton SA, Sikes JL, Heath SC, Simantov R, Levin LF, Shu P, Moore KJ, Breslow JL, Smith JD. Genetic background determines the extent of atherosclerosis in ApoE-deficient mice. Arterioscler Thromb Vasc Biol 19: 1960-1968, 1999.
18. Delafontaine P, Song YH, Li Y. Expression, regulation, and function of IGF-1, IGF-1R, and IGF-1 binding proteins in blood vessels. Arterioscler Thromb Vasc Biol 24: 435-444, 2004. (Pubitemid 38326135)
19. Duan C, Hawes SB, Prevette T, Clemmons DR. Insulin-like growth factor-I (IGF-I) regulates IGF-binding protein-5 synthesis through transcriptional activation of the gene in aortic smooth muscle cells. J Biol Chem 271: 4280-4288, 1996. (Pubitemid 26070534)
20. Elesber AA, Lerman A, Denktas AE, Resch ZT, Bunch TJ, Schwartz RS, Conover CA. Pregnancy associated plasma protein-A and risk stratification of patients presenting with chest pain in the emergency department. Int J Cardiol 117: 365-369, 2007. (Pubitemid 46507629)
21. Harrington SC, Simari RD, Conover CA. Genetic deletion of pregnancy-associated plasma protein-A is associated with resistance to atherosclerotic lesion development in apolipoprotein E-deficient mice challenged with a high-fat diet. Circ Res 100: 1696-1702, 2007.
22. Heeschen C, Dimmeler S, Hamm CW, Fichtlscherer S, Simoons ML, Zeiher AM, CAPTURE Study Investigators. Pregnancy-associated plasma protein-A levels in patients with acute coronary syndromes: comparison with markers of systemic inflammation, platelet activation, and myocardial necrosis. J Am Coll Cardiol 45: 229-237, 2005. (Pubitemid 40094730)
23. Hochberg Z, Hertz P, Maor G, Oiknine J, Aviram M. Growth hormone and insulin-like growth factor-I increase macrophage uptake and degradation of low density lipoprotein. Endocrinology 131: 430-435, 1992.
24. Kumar A, Mohan S, Newton J, Rehage M, Tran K, Baylink DJ, Qin X. Pregnancy-associated plasma protein-A regulates myoblast proliferation and differentiation through an insulin-like growth factor-dependent mechanism. J Biol Chem 280: 37782-37789, 2005.
25. Laursen LS, Kjaer-Sorensen K, Andersen MH, Oxvig C. Regulation of insulin-like growth factor (IGF) bioactivity by sequential proteolytic cleavage of IGF binding protein-4 and -5. Mol Endocrinol 21: 1246-1257, 2007.
26. Laursen LS, Overgaard MT, Soe R, Boldt HB, Sottrup-Jensen L, Giudice LC, Conover CA, Oxvig C. Pregnancy-associated plasma protein-A (PAPP-A) cleaves insulin-like growth factor binding protein (IGFBP)-5 independent of IGF: implications for the mechanism of IGFBP-4 proteolysis by PAPP-A. FEBS Lett 504: 36-40, 2001.
27. Lawrence JB, Oxvig C, Overgaard MT, Sottrup-Jensen L, Gleich GJ, Hays LG, Yates JRIII, Conover CA. The insulin-like growth factor (IGF)-dependent IGF binding protein-4 protease secreted by human fibroblasts is pregnancy-associated plasma protein-A. Proc Natl Acad Sci USA 96: 3149-3153, 1999.
28. Li Li Miano JM, Mercer B, Olson EN. Expression of the SM22α promoter in transgenic mice provides evidence for distinct transcriptional regulatory programs in vascular and visceral smooth muscle cells. J Cell Biol 132: 849-859, 1996.
29. Lund J, Qin QP, Ilva T, Pettersson K, Voipio-Pulkki LM, Porela P, Pulkki K. Circulating pregnancy-associated plasma protein A predicts outcome in patients with acute coronary syndrome but no troponin I elevation. Circulation 108: 1924-1926, 2003.
30. Nakashima Y, Plump AS, Raines EW, Breslow JL, Ross R. ApoE-deficient mice develop lesions of all phases of atherosclerosis throughout the arterial tree. Arterioscler Thromb 14: 133-140, 1994.
31. Nichols TC, du Laney T, Zheng B, Bellinger DA, Nickols GA, Engleman W, Clemmons DR. Reduction in atherosclerotic lesion size in pigs by αVβ3 inhibitors is associated with inhibition of insulin-like growth factor-I-mediated signaling. Circ Res 85: 1040-1045, 1999.
32. Ning Y, Schuller AGP, Conover CA, Pintar JE. Insulin-like growth factor (IGF) binding protein-4 is both a positive and negative regulator of IGF activity in vivo. Mol Endocrinol 22: 1213-1225, 2008.
33. Okura Y, Brink M, Zahid AA, Anwar A, Delafontaine P. Decreased expression of insulin-like growth factor-1 and apoptosis of vascular smooth muscle cells in human atherosclerotic plaque. J Mol Cell Cardiol 33: 1777-1789, 2001.
34. Overgaard MT, Haaning J, Boldt HB, Olsen IM, Laursen LS, Christiansen M, Gleich GJ, Sottrup-Jensen L, Conover CA, Oxvig C. Expression of recombinant human pregnancy-associated plasma protein-A and identification of the proform of eosinophil major basic protein as its physiological inhibitor. J Biol Chem 275: 31128-31133, 2000.
35. Owens GK. Regulation of differentiation of vascular smooth muscle cells. Physiol Rev 75: 487-517, 1995.
36. Plump AS, Smith JD, Hayek T, Aalto-Setala K, Walsh A, Verstuyft JG, Rubin EM, Breslow JL. Severe hypercholesterolemia and atherosclerosis in apolipoprotein E-deficient mice created by homologous recombination in ES cells. Cell 71: 343-353, 1992.
37. Qin X, Byun D, Lau KH, Baylink DJ, Mohan S. Evidence that the interaction between insulin-like growth factor (IGF)-II and IGF binding protein (IGFBP)-4 is essential for the action of the IGF-II-dependent IGFBP-4 protease. Arch Biochem Biophys 379: 209-216, 2000.
38. Qin X, Wergedal JE, Rehage M, Tran K, Newton J, Lam P, Baylink DJ, Mohan S. Pregnancy-associated plasma protein-A increases osteoblast proliferation in vitro and bone formation in vivo. Endocrinology 147: 5653-5661, 2006.
39. Reddick RL, Zhang SH, Maeda N. Atherosclerosis in mice lacking Apo E: evaluation of lesional development and progression. J Atheroscler Thromb 14: 141-147, 1994.
40. Regan CP, Adam PJ, Madsen CS, Owens GK. Molecular mechanisms of decreased smooth muscle differentiation marker expression after vascular injury. J Clin Invest 106: 1139-1147, 2000.
41. Resch ZT, Simari RD, Conover CA. Targeted disruption of the PAPP-A gene is associated with diminished smooth muscle cell response to insulin-like growth factor-I and resistance to neointimal hyperplasia following vascular injury. Endocrinology 147: 5634-5640, 2006.
42. Smith JD, Breslow JL. The emergence of mouse models of atherosclerosis and their relevance to clinical research. J Intern Med 242: 99-109, 1997.
43. Smith EP, Kamyar A, Niu W, Wang J, Cercek B, Chernausek SD, Fagin JA. IGF-binding protein-4 expression and IGF-binding protein-4 protease activity are regulated coordinately in smooth muscle during postnatal development and after vascular injury. Endocrinology 142: 4420-4427, 2001.
44. Soe R, Overgaard MT, Thomsen AR, Laursen LS, Olsen IM, Sottrup-Jensen L, Haaning J, Giudice LC, Conover CA, Oxvig C. Expression of recombinant murine pregnancy-associated plasma protein-A (PAPP-A) and a novel variant (PAPP-Ai) with differential proteolytic activity. Eur J Biochem 269: 2247-2256, 2002.
45. Sukhanov S, Higashi Y, Shai SY, Vaughn C, Mohler J, Li Y, Song YH, Titterington J, Delafontaine P. IGF-1 reduces inflammatory responses, suppresses oxidative stress, and decreases atherosclerosis progression in ApoE-deficient mice. Arterioscler Thromb Vasc Biol 27: 2684-2690, 2007.
46. Thorn EM, Khan IA. Pregnancy-associated plasma protein-A: an emerging cardiac biomarker. Int J Cardiol 117: 370-372, 2007.
47. Wamhoff BR, Hoofnagle MH, Burns A, Sinha S, McDonald OG, Owens GK. A G/C element mediates repression of the SM22α promoter within phenotypically modulated smooth muscle cells in experimental atherosclerosis. Circ Res 95: 981-988, 2004.
48. Wang J, Niu W, Nikiforov Y, Naito S, Chernausek S, Witte D, LeRoith D, Strauch A, Fagin JA. Targeted overexpression of IGF-I evokes distinct patterns of organ remodeling in smooth muscle cell tissue beds of transgenic mice. J Clin Invest 100: 1425-1439, 1997.
49. Wang J, Niu W, Witte DP, Chernausek SD, Nikiforov YE, Clemens TL, Sharifi B, Straugh AR, Fagin JA. Overexpression of insulin-like growth factor-binding protein-4 (IGFBP-4) in smooth muscle cells of transgenic mice through a smooth muscle α-actin-IGFBP-4 fusion gene induces smooth muscle hypoplasia. Endocrinology 139: 2605-2614, 1998.
50. Ye P, D'Ercole J. Insulin-like growth factor (IGF-I) regulates IGF binding protein-5 gene expression in the brain. Endocrinology 139: 65-71, 1998.
51. Zhang M, Smith EP, Kuroda H, Banach W, Chernausek SD, Fagin JA. Targeted expression of a protease-resistant IGFBP-4 mutant in smooth muscle of transgenic mice results in IGFBP-4 stabilization and smooth muscle hypotrophy. J Biol Chem 277: 21285-21290, 2002.