MFG-E8 activates proliferation of vascular smooth muscle cells via integrin signaling

Aging Cell

Volumn 11, Issue 3, 2012, Pages 500-508

  Wang, Mingyi ^a   Fu, Zongming ^b   Wu, James ^a   Zhang, Jing ^a   Jiang, Liqun ^a   Khazan, Benjamin ^a   Telljohann, Richard ^a   Zhao, Mingming ^a   Krug, Alexander W ^a   Pikilidou, Maria ^a   Monticone, Robert E ^a   Wersto, Robert ^a   Van Eyk, Jennifer ^b   Lakatta, Edward G ^a  

^a NATIONAL INSTITUTE ON AGING   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Aging; Cell cycle; MFG E8; Vascular remodeling; VSMC proliferation

Indexed keywords

ALPHAVBETA5 INTEGRIN; MILK FAT GLOBULE EPIDERMAL GROWTH FACTOR 8 PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 1; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTERY WALL; ARTICLE; CELL ACTIVATION; CELL CYCLE; CELL CYCLE G0 PHASE; CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; CELL CYCLE S PHASE; CELL INVASION; CELL PROLIFERATION; CONTROLLED STUDY; IN VITRO STUDY; IN VIVO STUDY; MALE; MOLECULAR MECHANICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; RAT; VASCULAR SMOOTH MUSCLE;

AGE FACTORS; ANIMALS; ANTIGENS, SURFACE; CELL GROWTH PROCESSES; IMMUNOHISTOCHEMISTRY; INTEGRINS; MALE; MAP KINASE SIGNALING SYSTEM; MILK PROTEINS; MUSCLE, SMOOTH, VASCULAR; PHOSPHORYLATION; PLATELET-DERIVED GROWTH FACTOR; RATS; RATS, INBRED BN; RATS, INBRED F344; RATS, SPRAGUE-DAWLEY;

RATTUS;

EID: 84860883438     PISSN: 14749718     EISSN: 14749726     Source Type: Journal    
DOI: 10.1111/j.1474-9726.2012.00813.x     Document Type: Article

References (45)

1. Bagnato C, Thumar J, Mayya V, Hwang SI, Zebroski H, Claffey KP, Haudenschild C, Eng JK, Lundgren DH, Han DK (2007) Proteomics analysis of human coronary atherosclerotic plaque: a feasibility study of direct tissue proteomics by liquid chromatography and tandem mass spectrometry. Mol. Cell. Proteomics 6, 1088-1102.
2. Banai S, Wolf Y, Golomb G, Pearle A, Waltenberger J, Fishbein I, Schneider A, Gazit A, Perez L, Huber R, Lazarovichi G, Rabinovich L, Levitzki A, Gertz SD (1998) PDGF-receptor tyrosine kinase blocker AG1295 selectively attenuates smooth muscle cell growth in vitro and reduces neointimal formation after balloon angioplasty in swine. Circulation 97, 1960-1969.
3. Bondjers C, Kalén M, Hellström M, Scheidl SJ, Abramsson A, Renner O, Lindahl P, Cho H, Kehrl J, Betsholtz C (2003) Transcription profiling of platelet-derived growth factor-B-deficient mouse embryos identifies RGS5 as a novel marker for pericytes and vascular smooth muscle cells. Am. J. Pathol. 162, 721-729.
4. Braden WA, McClendon AK, Knudsen ES (2008) Cyclin-dependent kinase 4/6 activity is a critical determinant of pre-replication complex assembly. Oncogene 27, 7083-7093.
5. Bu HF, Zuo XL, Wang X, Ensslin MA, Koti V, Hsueh W, Raymond AS, Shur BD, Tan XD (2007) Milk fat globule-EGF factor 8/lactadherin plays a crucial role in maintenance and repair of murine intestinal epithelium. J. Clin. Invest. 117, 3673-3683.
6. Burgess BL, Abrams TA, Nagata S, Hall MO (2006) MFG-E8 in the retina and retinal pigment epithelium of rat and mouse. Mol. Vis. 12, 1437-1447.
7. Carrascosa C, Obula RG, Missiaglia E, Lehr HA, Delorenzi M, Frattini M, Rüegg C, Mariotti A (2011) MFG-E8/lactadherin regulates cyclins D1/D3 expression and enhances the tumorigenic potential of mammary epithelial cells. Oncogene. DOI:.
8. Ding L, Chapman A, Boyd R, Wang HD (2007) ERK activation contributes to regulation of spontaneous contractile tone via superoxide anion in isolated rat aorta of angiotensin II-induced hypertension. Am. J. Physiol. Heart Circ. Physiol. 292, H2997-H3005.
9. Ensslin MA, Shur BD (2007) The EGF repeat and discoidin domain protein, SED1/MFG-E8, is required for mammary gland branching morphogenesis. Proc. Natl Acad. Sci. U S A. 104, 2715-2720.
10. Fingerle J, Johnson R, Clowes AW, Majesky MW, Reidy MA (1989) Role of platelets in smooth muscle cell proliferation and migration after vascular injury in rat carotid artery. Proc. Natl Acad. Sci. U S A. 86, 8412-8416.
11. Fu Z, Wang M, Gucek M, Zhang J, Wu J, Jiang L, Monticone RE, Khazan B, Telljohann R, Mattison J, Sheng S, Cole RN, Spinetti G, Pintus G, Liu L, Kolodgie FD, Virmani R, Spurgeon H, Ingram DK, Everett AD, Lakatta EG, Van Eyk JE (2009) Milk fat globule protein-epidermal growth factor-8: a pivotal relay element within the angiotensin II and monocyte chemoattractant protein-1 signaling cascade mediating vascular smooth muscle cells invasion. Circ. Res. 104, 1337-1346.
12. Gerdes J, Schwab U, Lemke H, Stein H (1983) Production of a mouse monoclonal antibody reactive with a human nuclear antigen associated with cell proliferation. Int. J. Cancer 31, 13-20.
13. Hall PA, Levison DA, Woods AL, Yu CC-W, Kellock DB, Watkins JA, Barnes DM, Gillett CE, Camplejohn R, Dover R, Waseem NH, Lane DP (1990) Proliferating cell nuclear antigen (PCNA) immunolocalization in paraffin sections: an index of cell proliferation with evidence of deregulated expression in some neoplasms. J. Pathol. 162, 285-294.
14. Hariri R, Hajjar DP, Coletti D, Alonso DR, Weksler ME, Rabellino E (1988) Aging and arteriosclerosis: cell cycle kinetics of young and old arterial smooth muscle cells. Am. J. Pathol. 131, 132-136.
15. Jiang L, Wang M, Zhang J, Monticone RE, Telljohann R, Spinetti G, Pintus G, Lakatta EG (2008) Increased aortic calpain-1 activity mediates age-associated angiotensin II signaling of vascular smooth muscle cells. PLoS ONE 3, e2231.
16. Jinushi M, Nakazaki Y, Carrasco DR, Draganov D, Souders N, Johnson M, Mihm MC, Dranoff G (2008) Milk fat globule EGF-8 promotes melanoma progression through coordinated Akt and twist signaling in the tumor microenvironment. Cancer Res. 68, 8889-88898.
17. Jinushi M, Sato M, Kanamoto A, Itoh A, Nagai S, Koyasu S, Dranoff G, Tahara H (2009) Milk fat globule epidermal growth factor-8 blockade triggers tumor destruction through coordinated cell-autonomous and immune-mediated mechanisms. J. Exp. Med. 206, 1317-1326.
18. Ju H, Gros R, You X, Tsang S, Husain M, Rabinovitch M (2001) Conditional and targeted overexpression of vascular chymase causes hypertension in transgenic mice. Proc. Natl Acad. Sci. U S A. 98, 7469-7474.
19. Lakatta EG, Levy D (2003) Arterial and cardiac aging: major shareholders in cardiovascular disease enterprises: part I: aging arteries: a "set up" for vascular disease. Circulation 107, 139-146.
20. Lakatta EG, Wang M, Najjar SS (2009) Arterial aging and subclinical arterial disease are fundamentally intertwined at macroscopic and molecular levels. Med. Clin. North Am. 93, 583-604.
21. Lee SJ, Kim WJ, Moon SK (2009) TNF-alpha regulates vascular smooth muscle cell responses in genetic hypertension. Int. Immunopharmacol. 9, 837-843.
22. Li Z, Cheng H, Lederer WJ, Froehlich J, Lakatta EG (1997) Enhanced proliferation and migration and altered cytoskeletal proteins in early passage smooth muscle cells from young and old rat aortic explants. Exp. Mol. Pathol. 64, 1-11.
23. Li XL, Li BY, Gao HQ, Cheng M, Xu L, Li XH, Zhang WD, Hu JW (2010) Proteomics approach to study the mechanism of action of grape seed proanthocyanidin extracts on arterial remodeling in diabetic rats. Int. J. Mol. Med. 25, 237-248.
24. Lin YP, Hsu ME, Chiou YY, Hsu HY, Tsai HC, Peng YJ, Lu CY, Pan CY, Yu WC, Chen CH, Chi CW, Lin CH (2010) Comparative proteomic analysis of rat aorta in a subtotal nephrectomy model. Proteomics 10, 2429-2443.
25. Marrero MB, Schieffer B, Li B, Sun J, Harp JB, Ling BN (1997) Role of Janus kinase/signal transducer and activator of transcription and mitogen-activated protein kinase cascades in angiotensin II- and platelet-derived growth factor-induced vascular smooth muscle cell proliferation. J. Biol. Chem. 272, 24684-24690.
26. McCaffrey TA, Nicholson AC, Szabo PE, Weksler ME, Weksler BB (1988) Aging and arteriosclerosis. The increased proliferation of arterial smooth muscle cells isolated from old rats is associated with increased platelet-derived growth factor-like activity. J. Exp. Med. 167, 163-174.
27. Motegi SI, Garfield S, Feng X, Sárdy M, Udey MC (2011a) Potentiation of platelet-derived growth factor receptor-{beta} signaling mediated by integrin-associated MFG-E8. Arterioscler. Thromb. Vasc. Biol. 31, 2653-2664.
28. Motegi S, Leitner WW, Lu M, Tada Y, Sárdy M, Wu C, Chavakis T, Udey MC (2011b) Pericyte-derived MFG-E8 regulates pathologic angiogenesis. Arterioscler. Thromb. Vasc. Biol. 31, 2024-2034.
29. Neutzner M, Lopez T, Feng X, Bergmann-Leitner ES, Leitner WW, Udey MC (2007) MFG-E8/lactadherin promotes tumor growth in an angiogenesis-dependent transgenic mouse model of multistage carcinogenesis. Cancer Res. 67, 6777-6785.
30. Okuyama T, Kurata S, Tomimori Y, Fukunishi N, Sato S, Osada M, Tsukinoki K, Jin HF, Yamashita A, Ito M, Kobayashi S, Hata RI, Ikawa Y, Katoh I (2008) p63(TP63) elicits strong trans-activation of the MFG-E8/lactadherin/BA46 gene through interactions between the TA and DeltaN isoforms. Oncogene 27, 308-317.
31. Rao HV, Thirumangalakudi L, Desmond P, Grammas P (2007) Cyclin D1, cdk4, and Bim are involved in thrombin-induced apoptosis in cultured cortical neurons. J. Neurochem. 101, 498-505.
32. Scheidl SJ, Nilsson S, Kalén M, Hellström M, Takemoto M, Håkansson J, Lindahl P (2002) mRNA expression profiling of laser microbeam microdissected cells from slender embryonic structures. Am. J. Pathol. 160, 801-813.
33. Shapiro PS, Vaisberg E, Hunt AJ, Tolwinski NS, Whalen AM, McIntosh JR, Ahn NG (1998) Activation of the MKK/ERK pathway during somatic cell mitosis: direct interactions of active ERK with kinetochores and regulation of the mitotic 3F3/2 phosphoantigen. J. Cell Biol. 142, 1533-1545.
34. Silvestre JS, Thery C, Hamard G, Boddaert J, Aguilar B, Delcayre A, Houbron C, Tamarat R, Blanc-Brude O, Heeneman S, Clergue M, Duriez M, Merval R, Levy B, Tedgui A, Amigorena S, Mallat Z (2005) Lactadherin promotes VEGF-dependent neovascularization. Nat. Med. 11, 499-506.
35. Spinetti G, Wang M, Monticone RE, Zhang J, Zhao D, Lakatta EG (2004) Rat aortic MCP-1 and its receptor CCR2 increase with age and alter vascular smooth muscle cell function. Arterioscler. Thromb. Vasc. Biol. 24, 1397-1402.
36. Taylor MR, Couto JR, Scallan CD, Ceriani RL, Peterson JA (1997) Lactadherin (formerly BA46), a membrane-associated glycoprotein expressed in human milk and breast carcinomas, promotes Arg-Gly-Asp (RGD)-dependent cell adhesion. DNA Cell Biol. 16, 861-869.
37. Wang M, Lakatta EG (2002) Altered regulation of matrix metalloproteinase-2 in aortic remodeling during aging. Hypertension 39, 865-873.
38. Wang M, Takagi G, Asai K, Resuello RG, Natividad FF, Vatner DE, Vatner SF, Lakatta EG (2003) Aging increases aortic MMP-2 activity and angiotensin II in nonhuman primates. Hypertension 41, 1308-1316.
39. Wang M, Zhang J, Spinetti G, Jiang L, Monticone R, Zhao D, Cheng L, Krawczyk M, Talan M, Pintus G, Lakatta EG (2005) Angiotensin II activates matrix metalloproteinase type II and mimics age-associated carotid arterial remodeling in young rats. Am. J. Pathol. 167, 1429-1442.
40. Wang M, Zhao D, Spinetti G, Zhang J, Jiang LQ, Pintus G, Monticone R, Lakatta EG (2006) Matrix metalloproteinase 2 activation of transforming growth factor-beta1 (TGF-beta1) and TGF-beta1-type II receptor signaling within the aged arterial wall. Arterioscler. Thromb. Vasc. Biol. 26, 1503-1509.
41. Wang M, Zhang J, Jiang LQ, Spinetti G, Pintus G, Monticone R, Kolodgie FD, Virmani R, Lakatta EG (2007) Proinflammatory profile within the grossly normal aged human aortic wall. Hypertension 50, 219-227.
42. Wang M, Monticone RE, Lakatta EG (2010) Arterial aging: a journey into subclinical arterial disease. Curr. Opin. Nephrol. Hypertens. 19, 201-207.
43. Wang M, Spinetti G, Monticone R, Zhang J, Pintus G, Jiang LQ, Lakatta EG (2011) A local proinflammation signaling loop facilitates adverse aging-associated arterial remodeling. PLoS ONE 6, e16653.
44. Yang C, Hayashida T, Forster N, Li C, Shen D, Maheswaran S, Chen L, Anderson KS, Ellisen LW, Sgroi D, Schmidt EV (2011) The integrin alpha(v)beta(3-5) ligand MFG-E8 is a p63/p73 target gene in triple-negative breast cancers but exhibits suppressive functions in ER(+) and erbB2(+) breast cancers. Cancer Res. 71, 937-945.
45. Zeelenberg IS, Ostrowski M, Krumeich S, Bobrie A, Jancic C, Boissonnas A, Delcayre A, Le Pecq JB, Combadière B, Amigorena S, Théry C (2008) Targeting tumor antigens to secreted membrane vesicles in vivo induces efficient antitumor immune responses. Cancer Res. 68, 1228-1235.