Endothelial-derived neuregulin is an important mediator of ischaemia-induced angiogenesis and arteriogenesis

Cardiovascular Research

Volumn 93, Issue 3, 2012, Pages 516-524

  Hedhli, Nadia ^a   Dobrucki, Lawrence W ^a   Kalinowski, April ^a   Zhuang, Zhen W ^a   Wu, Xiaohong ^a   Russell III, Raymond R ^a   Sinusas, Albert J ^a   Russell, Kerry S ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Angiogenesis; Endothelium; Genetically altered mice; Growth factors; Ischaemia

Indexed keywords

NEU DIFFERENTIATION FACTOR; VITRONECTIN RECEPTOR;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTERY LIGATION; ARTICLE; AUTONOMIC NERVOUS SYSTEM FUNCTION; CAPILLARY DENSITY; CONTROLLED STUDY; FEMORAL ARTERY; HEART MUSCLE ISCHEMIA; MOUSE; NONHUMAN; PRIORITY JOURNAL; VASCULAR ENDOTHELIUM;

ANIMALS; AORTA, THORACIC; BIOCOMPATIBLE MATERIALS; CELL DIVISION; COLLAGEN; DISEASE MODELS, ANIMAL; DRUG COMBINATIONS; ENDOTHELIUM, VASCULAR; FEMORAL ARTERY; GENE EXPRESSION; HUMANS; INTEGRIN ALPHAVBETA3; ISCHEMIA; LAMININ; MICE; MICE, KNOCKOUT; NEOVASCULARIZATION, PHYSIOLOGIC; NEUREGULIN-1; PROTEOGLYCANS; RECOMBINANT PROTEINS; REGIONAL BLOOD FLOW;

EID: 84863265688     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvr352     Document Type: Article

References (37)

1. Iivanainen E, Paatero I, Heikkinen SM, Junttila TT, Cao R, Klint P et al. Intra-and extracellular signaling by endothelial neuregulin-1. Exp Cell Res 2007;313:2896-2909.
2. Olayioye MA, Neve RM, Lane HA, Hynes NE. The ErbB signaling network: receptor heterodimerization in development and cancer. EMBO J 2000;19:3159-3167.
3. Dankort DL, Muller WJ. Signal transduction in mammary tumorigenesis: a transgenic perspective. Oncogene 2000;19:1038-1044.
4. Piccart-Gebhart MJ, Procter M, Leyland-Jones B, Goldhirsch A, Untch M, Smith I et al. Trastuzumab after adjuvant chemotherapy in HER2-positive breast cancer. N Engl J Med 2005;353:1659-1672.
5. Loureiro RM, Maharaj AS, Dankort D, Muller WJ, D'Amore PA. ErbB2 overexpression in mammary cells upregulates VEGF through the core promoter. Biochem Biophys Res Commun 2005;326:455-465.
6. Russell KS, Stern DF, Polverini PJ, Bender JR. Neuregulin activation of ErbB receptors in vascular endothelium leads to angiogenesis. Am J Physiol 1999;277:H2205-2211.
7. Kalinowski A, Plowes NJ, Huang Q, Berdejo-Izquierdo C, Russell RR, Russell KS. Metalloproteinase-dependent cleavage of neuregulin and autocrine stimulation of vascular endothelial cells. FASEB J 2010;24:2567-2575.
8. Hedhli N, Huang Q, Kalinowski A, Palmeri M, Hu X, Russell RR et al. Endotheliumderived neuregulin protects the heart against ischemic injury. Circulation 2011;123:2254-2262.
9. Metzger D, Chambon P. Site-and time-specific gene targeting in the mouse. Methods 2001;24:71-80.
10. Bersell K, Arab S, Haring B, Kuhn B. Neuregulin1/ErbB4 signaling induces cardiomyocyte proliferation and repair of heart injury. Cell 2009;138:257-270.
11. Monvoisin A, Alva JA, Hofmann JJ, Zovein AC, Lane TF, Iruela-Arispe ML. VE-cadherin-CreERT2 transgenic mouse: a model for inducible recombination in the endothelium. Dev Dyn 2006;235:3413-3422.
12. Novak A, Guo C, Yang W, Nagy A, Lobe CG. Z/EG, a double reporter mouse line that expresses enhanced green fluorescent protein upon Cre-mediated excision. Genesis 2000;28:147-155.
13. Yang X, Arber S, William C, Li L, Tanabe Y, Jessell TM et al. Patterning of muscle acetylcholine receptor gene expression in the absence of motor innervation. Neuron 2001;30:399-410.
14. Ackah E, Yu J, Zoellner S, Iwakiri Y, Skurk C, Shibata R et al. Akt1/protein kinase Balpha is critical for ischemic and VEGF-mediated angiogenesis. J Clin Invest 2005;115:2119-2127.
15. Meoli DF, Sadeghi MM, Krassilnikova S, Bourke BN, Giordano FJ, Dione DP et al. Noninvasive imaging of myocardial angiogenesis following experimental myocardial infarction. J Clin Invest 2004;113:1684-1691.
16. Dobrucki LW, Dione DP, Kalinowski L, Dione D, Mendizabal M, Yu J et al. Serial noninvasive targeted imaging of peripheral angiogenesis: validation and application of a semiautomated quantitative approach. J Nucl Med 2009;50:1356-1363.
17. Zagorchev L, Oses P, Zhuang ZW, Moodie K, Mulligan-Kehoe MJ, Simons M et al. Micro computed tomography for vascular exploration. J Angiogenes Res 2010;2:7.
18. Zhuang ZW, Gao L, Murakami M, Pearlman JD, Sackett TJ, Simons M et al. Arteriogenesis: noninvasive quantification with multi-detector row CT angiography and three-dimensional volume rendering in rodents. Radiology 2006;240:698-707.
19. Lanahan AA, Chittenden TW, Mulvihill E, Smith K, Schwartz S, Simons M. Synectindependent gene expression in endothelial cells. Physiol Genomics 2006;27:380-390.
20. Yu J, Lei L, Liang Y, Hinh L, Hickey RP, Huang y et al. An engineered VEGF-activating zinc finger protein transcription factor improves blood flow and limb salvage in advanced-age mice. FASEB J 2006;20:479-481.
21. Guo W, Pylayeva Y, Pepe A, Yoshioka T, Muller WJ, Inghirami G et al. Beta 4 integrin amplifies ErbB2 signaling to promote mammary tumorigenesis. Cell 2006;126:489-502.
22. Brooks PC, Clark RA, Cheresh DA. Requirement of vascular integrin alpha v beta 3 for angiogenesis. Science 1994;264:569-571.
23. Menendez JA, Mehmi I, Griggs DW, Lupu R. The angiogenic factor CYR61 in breast cancer: molecular pathology and therapeutic perspectives. Endocr Relat Cancer 2003;10:141-152.
24. 99mTc-labeled peptide targeted at alphavbeta3 integrin after murine hindlimb ischemia. Circulation 2005;111:3255-3260.
25. Munoz-Chapuli R, Quesada AR, Angel Medina M. Angiogenesis and signal transduction in endothelial cells. Cell Mol Life Sci 2004;61:2224-2243.
26. Soldi R, Mitola S, Strasly M, Defilippi P, Tarone G, Bussolino F. Role of alphavbeta3 integrin in the activation of vascular endothelial growth factor receptor-2. EMBO J 1999;18:882-892.
27. Sheppard D. Endothelial integrins and angiogenesis: not so simple anymore. J Clin Invest 2002;110:913-914.
28. O'Kelly J, Chung A, Lemp N, Chumakova K, Yin D, Wang HJ et al. Functional domains of CCN1 (Cyr61) regulate breast cancer progression. Int J Oncol 2008;33:59-67.
29. Ieguchi K, Fujita M, Ma Z, Davari P, Taniguchi Y, Sekiguchi K et al. Direct binding of the EGF-like domain of neuregulin-1 to integrins ({alpha}v{beta}3 and {alpha}6{beta}4) is involved in neuregulin-1/ErbB signaling. J Biol Chem 2010;285:31388-31398.
30. Soung YH, Clifford JL, Chung J. Crosstalk between integrin and receptor tyrosine kinase signaling in breast carcinoma progression. BMB Rep 2010;43:311-318.
31. Kuramochi Y, Cote GM, Guo X, Lebrasseur NK, Cui L, Liao R et al. Cardiac endothelial cells regulate reactive oxygen species-induced cardiomyocyte apoptosis through neuregulin-1beta/erbB4 signaling. J Biol Chem 2004;279:51141-51147.
32. Wragg A, Mellad JA, Beltran LE, Konoplyannikov M, San H, Boozer S et al. VEGFR1/CXCR4-positive progenitor cells modulate local inflammation and augment tissue perfusion by a SDF-1-dependent mechanism. J Mol Med 2008;86:1221-1232.
33. Luft FC. Mononuclear inflammatory cells and angiogenesis. J Mol Med 2008;86:1193-1195.
34. Safa RN, Peng XY, Pentassuglia L, Lim CC, Lamparter M, Silverstein C et al. Neuregulin-1beta regulation of embryonic endothelial progenitor cell survival. Am J Physiol Heart Circ Physiol 2011;300:H1311-1319.
35. Kalinowski A, Hedhli N, Russell KS. Vascular smooth muscle cells express ErbB receptors and migrate in response to neuregulin. Circulation 2009;120:S1168b.
36. Iivanainen E, Nelimarkka L, Elenius V, Heikkinen SM, Junttila TT, Sihombing L et al. Angiopoietin-regulated recruitment of vascular smooth muscle cells by endothelialderived heparin binding EGF-like growth factor. FASEB J 2003;17:1609-1621.
37. Bagheri-Yarmand R, Vadlamudi RK, Wang RA, Mendelsohn J, Kumar R. Vascular endothelial growth factor up-regulation via p21-activated kinase-1 signaling regulates heregulin-beta1-mediated angiogenesis. J Biol Chem 2000;275:39451-39457.