Secreted Frizzled-related protein 2 as a target in antifibrotic therapeutic intervention

American Journal of Physiology - Cell Physiology

Volumn 306, Issue 6, 2014, Pages

  Mastri, Michalis ^a   Shah, Zaeem ^a   Hsieh, Karin ^a   Wang, Xiaowen ^a   Wooldridge, Bailey ^a   Martin, Sean ^a   Suzuki, Gen ^a   Lee, Techung ^a  

^a University at Buffalo SUNY   (United States)

Author keywords

Fibrosis; Heart failure; MMP; VEGF

Indexed keywords

ANTIFIBROTIC AGENT; AXIN; AXIN 2; GELATINASE A; IMMUNOGLOBULIN G; PROTEIN ANTIBODY; SCATTER FACTOR; SECRETED FRIZZLED RELATED PROTEIN 2; SECRETED FRIZZLED RELATED PROTEIN 2 ANTIBODY; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR GATA 4; TRANSCRIPTION FACTOR MEF2C; UNCLASSIFIED DRUG; VASCULOTROPIN; ANTIBODY; MEMBRANE PROTEIN; SFRP2 PROTEIN, MOUSE; VASCULOTROPIN A;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CARDIOMYOPATHY; CONTROLLED STUDY; DRUG MECHANISM; DRUG TARGETING; ECHOCARDIOGRAPHY; ENZYME ACTIVITY; GENE EXPRESSION; HAMSTER MODEL; HEART LEFT VENTRICLE EJECTION FRACTION; HEART MUSCLE FIBROSIS; HISTOLOGY; MALE; MESENCHYMAL STEM CELL TRANSPLANTATION; MYOFIBROBLAST; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; ANIMAL; BAGG ALBINO MOUSE; CELL CULTURE; FIBROSIS; HAMSTER; HEART; HEART FAILURE; HEART INFARCTION; HEART LEFT VENTRICLE FUNCTION; HEART MUSCLE; HEART STROKE VOLUME; IMMUNOLOGY; METABOLISM; MMP; MOUSE; PATHOLOGY; PHYSIOLOGY; SECRETION (PROCESS); SFRP2; SIGNAL TRANSDUCTION;

FIBROSIS; HEART FAILURE; MMP; SFRP2; VEGF;

ANIMALS; ANTIBODIES; APOPTOSIS; AXIN PROTEIN; CELLS, CULTURED; CRICETINAE; FIBROSIS; HEART; HEART FAILURE; HEPATOCYTE GROWTH FACTOR; MALE; MATRIX METALLOPROTEINASE 2; MEMBRANE PROTEINS; MICE; MICE, INBRED BALB C; MYOCARDIAL INFARCTION; MYOCARDIUM; NEOVASCULARIZATION, PHYSIOLOGIC; SIGNAL TRANSDUCTION; STROKE VOLUME; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VENTRICULAR FUNCTION, LEFT;

EID: 84900032926     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00238.2013     Document Type: Article

References (71)

1. Alfaro MP, Vincent A, Saraswati S, Thorne CA, Hong CC, Lee E, Young PP. sFRP2 suppression of bone morphogenic protein (BMP) and Wnt signaling mediates mesenchymal stem cell (MSC) self-renewal promoting engraftment and myocardial repair. J Biol Chem 285: 35645-35653, 2010.
2. Bai L, Lennon DP, Caplan AI, Dechant A, Hecker J, Kranso J, Zaremba A, Miller RH. Hepatocyte growth factor mediates mesenchymal stem cell-induced recovery in multiple sclerosis models. Nat Neurosci 15: 862-870, 2012.
3. Biernacka A, Frangogiannis NG. Aging and cardiac fibrosis. Aging Dis 2: 158-173, 2011.
4. Bovolenta P, Esteve P, Ruiz JM, Cisneros E, Lopez-Rios J. Beyond Wnt inhibition: new functions of secreted Frizzled-related proteins in development and disease. J Cell Sci 121: 737-746, 2008.
5. Cheng YY, Yu J, Wong YP, Man EP, To KF, Jin VX, Li J, Tao Q, Sung JJ, Chan FK, Leung WK. Frequent epigenetic inactivation of secreted frizzled-related protein 2 (SFRP2) by promoter methylation in human gastric cancer. Br J Cancer 97: 895-901, 2007.
6. Coussens LM, Fingleton B, Matrisian LM. Matrix metalloproteinase inhibitors and cancer: trials and tribulations. Science 295: 2387-2392, 2002.
7. Delgado MB, Clark-Lewis I, Loetscher P, Langen H, Thelen M, Baggiolini M, Wolf M. Rapid inactivation of stromal cell-derived factor-1 by cathepsin G associated with lymphocytes. Eur J Immunol 31: 699-707, 2001.
8. Dobaczewski M, Frangogiannis NG. Chemokines and cardiac fibrosis. Front Biosci 1: 391-405, 2009.
9. Esteve P, Sandonis A, Cardozo M, Malapeira J, Ibanez C, Crespo I, Marcos S, Gonzalez-Garcia S, Toribio ML, Arribas J, Shimono A, Guerrero I, Bovolenta P. SFRPs act as negative modulators of ADAM10 to regulate retinal neurogenesis. Nat Neurosci 14: 562-569, 2011.
10. Fedi P, Bafico A, Nieto Soria A, Burgess WH, Miki T, Bottaro DP, Kraus MH, Aaronson SA. Isolation and biochemical characterization of the human Dkk-1 homologue, a novel inhibitor of mammalian Wnt signaling. J Biol Chem 274: 19465-19472, 1999.
11. Folkman J. Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat Med 1: 27-31, 1995.
12. Gerritsen ME. HGF and VEGF: a dynamic duo. Circ Res 96: 272-273, 2005.
13. Goineau S, Pape D, Guillo P, Ramee MP, Bellissant E. Hemodynamic and histomorphometric characteristics of dilated cardiomyopathy of Syrian hamsters (Bio TO-2 strain). Can J Physiol Pharmacol 79: 329-337, 2001.
14. Goldsmith EC, Bradshaw AD, Spinale FG. Cellular mechanisms of tissue fibrosis. 2. Contributory pathways leading to myocardial fibrosis: moving beyond collagen expression. Am J Physiol Cell Physiol 304: C393-C402, 2013.
15. Hawwa RL, Hokenson MA, Wang Y, Huang Z, Sharma S, Sanchez-Esteban J. Differential expression of MMP-2 and-9 and their inhibitors in fetal lung cells exposed to mechanical stretch: regulation by IL-10. Lung 189: 341-349, 2011.
16. He W, Zhang L, Ni A, Zhang Z, Mirotsou M, Mao L, Pratt RE, Dzau VJ. Exogenously administered secreted frizzled related protein 2 (Sfrp2) reduces fibrosis and improves cardiac function in a rat model of myocardial infarction. Proc Natl Acad Sci USA 107: 21110-21115, 2010.
17. Hopkins DR, Keles S, Greenspan DS. The bone morphogenetic protein 1/Tolloid-like metalloproteinases. Matrix Biol 26: 508-523, 2007.
18. Houck KA, Leung DW, Rowland AM, Winer J, Ferrara N. Dual regulation of vascular endothelial growth factor bioavailability by genetic and proteolytic mechanisms. J Biol Chem 267: 26031-26037, 1992.
19. Hu J, Van den Steen PE, Sang QX, Opdenakker G. Matrix metalloproteinase inhibitors as therapy for inflammatory and vascular diseases. Nat Rev Drug Discov 6: 480-498, 2007.
20. Hudson PJ, Souriau C. Engineered antibodies. Nat Med 9: 129-134, 2003.
21. Iozzo RV, Zoeller JJ, Nystrom A. Basement membrane proteoglycans: modulators par excellence of cancer growth and angiogenesis. Mol Cells 27: 503-513, 2009.
22. Jho EH, Zhang T, Domon C, Joo CK, Freund JN, Costantini F. Wnt/ beta-catenin/Tcf signaling induces the transcription of Axin2, a negative regulator of the signaling pathway. Mol Cell Biol 22: 1172-1183, 2002.
23. Jugdutt BI. Limiting fibrosis after myocardial infarction. N Engl J Med 360: 1567-1569, 2009.
24. Jugdutt BI. Ventricular remodeling after infarction and the extracellular collagen matrix: when is enough enough? Circulation 108: 1395-1403, 2003.
25. Kanematsu A, Marui A, Yamamoto S, Ozeki M, Hirano Y, Yamamoto M, Ogawa O, Komeda M, Tabata Y. Type I collagen can function as a reservoir of basic fibroblast growth factor. J Control Release 99: 281-292, 2004.
26. Katoh M. Comparative genomics on SFRP2 orthologs. Oncol Rep 14: 783-787, 2005.
27. Keyt BA, Berleau LT, Nguyen HV, Chen H, Heinsohn H, Vandlen R, Ferrara N. The carboxyl-terminal domain (111-165) of vascular endothelial growth factor is critical for its mitogenic potency. J Biol Chem 271: 7788-7795, 1996.
28. Kobayashi K, Luo M, Zhang Y, Wilkes DC, Ge G, Grieskamp T, Yamada C, Liu TC, Huang G, Basson CT, Kispert A, Greenspan DS, Sato TN. Secreted Frizzled-related protein 2 is a procollagen C proteinase enhancer with a role in fibrosis associated with myocardial infarction. Nat Cell Biol 11: 46-55, 2009.
29. Kongkham PN, Northcott PA, Croul SE, Smith CA, Taylor MD, Rutka JT. The SFRP family of WNT inhibitors function as novel tumor suppressor genes epigenetically silenced in medulloblastoma. Oncogene 29: 3017-3024, 2010.
30. Kositprapa C, Zhang B, Berger S, Canty JMJ, Lee TC. Calpainmediated proteolytic cleavage of troponin I induced by hypoxia or metabolic inhibition in cultured neonatal cardiomyocytes. Mol Cell Biochem 214: 47-55, 2000.
31. Kress E, Rezza A, Nadjar J, Samarut J, Plateroti M. The frizzled-related sFRP2 gene is a target of thyroid hormone receptor alpha1 and activates beta-catenin signaling in mouse intestine. J Biol Chem 284: 1234-1241, 2009.
32. Leask A. Potential therapeutic targets for cardiac fibrosis: TGFbeta, angiotensin, endothelin, CCN2, and PDGF, partners in fibroblast activation. Circ Res 106: 1675-1680, 2010.
33. Lee T. Stem cell therapy independent of stemness. World J Stem Cells 4: 120-124, 2012.
34. Lin H, Shabbir A, Molnar M, Yang J, Marion S, Canty JMJ, Lee T. Adenoviral expression of vascular endothelial growth factor splice variants differentially regulate bone marrow-derived mesenchymal stem cells. J Cell Physiol 216: 458-468, 2008.
35. Markel TA, Wang Y, Herrmann JL, Crisostomo PR, Wang M, Novotny NM, Herring CM, Tan J, Lahm T, Meldrum DR. VEGF is critical for stem cell-mediated cardioprotection and a crucial paracrine factor for defining the age threshold in adult and neonatal stem cell function. Am J Physiol Heart Circ Physiol 295: H2308-H2314, 2008.
36. Mastri M, Shah Z, McLaughlin T, Greene CJ, Baum L, Suzuki G, Lee T. Activation of Toll-like receptor 3 (TLR3) amplifies mesenchymal stem cell trophic factors and enhances therapeutic potency. Am J Physiol Cell Physiol 303: C1021-C1033, 2012.
37. Minieri M, Fiaccavento R, Carosella L, Peruzzi G, Di Nardo P. The cardiomyopathic hamster as model of early myocardial aging. Mol Cell Biochem 198: 1-6, 1999.
38. Mirotsou M, Zhang Z, Deb A, Zhang L, Gnecchi M, Noiseux N, Mu H, Pachori A, Dzau V. Secreted frizzled related protein 2 (Sfrp2) is the key Akt-mesenchymal stem cell-released paracrine factor mediating myocardial survival and repair. Proc Natl Acad Sci USA 104: 1643-1648, 2007.
39. Missihoun C, Zisa D, Shabbir A, Lin H, Lee T. Myocardial oxidative stress, osteogenic phenotype, and energy metabolism are differentially involved in the initiation and early progression of delta-sarcoglycan-null cardiomyopathy. Mol Cell Biochem 321: 45-52, 2008.
40. Miura S, Ohno I, Suzuki J, Suzuki K, Okada S, Okuyama A, Nawata J, Ikeda J, Shirato K. Inhibition of matrix metalloproteinases prevents cardiac hypertrophy induced by beta-adrenergic stimulation in rats. J Cardiovasc Pharmacol 42: 174-181, 2003.
41. Moali C, Font B, Ruggiero F, Eichenberger D, Rousselle P, Francois V, Oldberg A, Bruckner-Tuderman L, Hulmes DJ. Substrate-specific modulation of a multisubstrate proteinase. C-terminal processing of fibrillar procollagens is the only BMP-1-dependent activity to be enhanced by PCPE-1. J Biol Chem 280: 24188-24194, 2005.
42. Muley A, Majumder S, Kolluru GK, Parkinson S, Viola H, Hool L, Arfuso F, Ganss R, Dharmarajan A, Chatterjee S. Secreted frizzled-related protein 4: an angiogenesis inhibitor. Am J Pathol 176: 1505-1516, 2010.
43. Musaro A, McCullagh K, Paul A, Houghton L, Dobrowolny G, Molinaro M, Barton ER, Sweeney HL, Rosenthal N. Localized Igf-1 transgene expression sustains hypertrophy and regeneration in senescent skeletal muscle. Nat Genet 27: 195-200, 2001.
44. Nathan E, Tzahor E. sFRPs: a declaration of (Wnt) independence. Nat Cell Biol 11: 13, 2009.
45. Neidhart M, Seemayer CA, Hummel KM, Michel BA, Gay RE, Gay S. Functional characterization of adherent synovial fluid cells in rheumatoid arthritis: destructive potential in vitro and in vivo. Arthritis Rheum 48: 1873-1880, 2003.
46. Ostrom RS. A new molecular target for blunting organ fibrosis. Focus on "Secreted Frizzled-related protein 2 as a target in antifibrotic therapeutic intervention. " Am J Physiol Cell Physiol (January 22, 2014). doi:10.1152/ ajpcell.00020.2014.
47. Park S, Kim ES, Noh DY, Hwang KT, Moon A. H-Ras-specific upregulation of granulocyte colony-stimulating factor promotes human breast cell invasion via matrix metalloproteinase-2. Cytokine 55: 126-133, 2011.
48. Petit I, Szyper-Kravitz M, Nagler A, Lahav M, Peled A, Habler L, Ponomaryov T, Taichman RS, Arenzana-Seisdedos F, Fujii N, Sandbank J, Zipori D, Lapidot T. G-CSF induces stem cell mobilization by decreasing bone marrow SDF-1 and up-regulating CXCR4. Nat Immunol 3: 687-694, 2002.
49. Ries C, Egea V, Karow M, Kolb H, Jochum M, Neth P. MMP-2, MT1-MMP, and TIMP-2 are essential for the invasive capacity of human mesenchymal stem cells: differential regulation by inflammatory cytokines. Blood 109: 4055-4063, 2007.
50. Ruiz V, Ordonez RM, Berumen J, Ramirez R, Uhal B, Becerril C, Pardo A, Selman M. Unbalanced collagenases/TIMP-1 expression and epithelial apoptosis in experimental lung fibrosis. Am J Physiol Lung Cell Mol Physiol 285: L1026-L1036, 2003.
51. Ryoke T, Gu Y, Mao L, Hongo M, Clark RG, Peterson KL, Ross J Jr. Progressive cardiac dysfunction and fibrosis in the cardiomyopathic hamster and effects of growth hormone and angiotensin-converting enzyme inhibition. Circulation 100: 1734-1743, 1999.
52. Schumann H, Holtz J, Zerkowski HR, Hatzfeld M. Expression of secreted frizzled related proteins 3 and 4 in human ventricular myocardium correlates with apoptosis related gene expression. Cardiovasc Res 45: 720-728, 2000.
53. Shabbir A, Zisa D, Lin H, Mastri M, Roloff G, Suzuki G, Lee T. Activation of host tissue trophic factors through JAK/STAT3 signaling: a mechanism of mesenchymal stem cell-mediated cardiac repair. Am J Physiol Heart Circ Physiol 299: H1428-H1438, 2010.
54. Shabbir A, Zisa D, Suzuki G, Lee T. Heart failure therapy mediated by the trophic activities of bone marrow mesenchymal stem cells: a noninvasive therapeutic regimen. Am J Physiol Heart Circ Physiol 296: H1888-H1897, 2009.
55. Singh M, Foster CR, Dalal S, Singh K. Osteopontin: role in extracellular matrix deposition and myocardial remodeling post-MI. J Mol Cell Cardiol 48: 538-543, 2010.
56. Spinale FG. Myocardial matrix remodeling and the matrix metalloproteinases: influence on cardiac form and function. Physiol Rev 87: 1285-1342, 2007.
57. Spinale FG, Janicki JS, Zile MR. Membrane-associated matrix proteolysis and heart failure. Circ Res 112: 195-208, 2013.
58. Toth M, Sohail A, Fridman R. Assessment of gelatinases (MMP-2 and MMP-9) by gelatin zymography. Meth Mol Biol 878: 121-135, 2012.
59. Upton Z, Cuttle L, Noble A, Kempf M, Topping G, Malda J, Xie Y, Mill J, Harkin DG, Kravchuk O, Leavesley DI, Kimble RM. Vitronectin: growth factor complexes hold potential as a wound therapy approach. J Invest Dermatol 128: 1535-1544, 2008.
60. Uren A, Reichsman F, Anest V, Taylor WG, Muraiso K, Bottaro DP, Cumberledge S, Rubin JS. Secreted frizzled-related protein-1 binds directly to Wingless and is a biphasic modulator of Wnt signaling. J Biol Chem 275: 4374-4382, 2000.
61. von Marschall Z, Fisher LW. Secreted Frizzled-related protein-2 (sFRP2) augments canonical Wnt3a-induced signaling. Biochem Biophys Res Commun 400: 299-304, 2010.
62. Weber KT, Sun Y, Bhattacharya SK, Ahokas RA, Gerling IC. Myofibroblast-mediated mechanisms of pathological remodelling of the heart. Nat Rev Cardiol 10: 15-26, 2013.
63. White LA, Mitchell TI, Brinckerhoff CE. Transforming growth factor beta inhibitory element in the rabbit matrix metalloproteinase-1 (collagenase-1) gene functions as a repressor of constitutive transcription. Biochim Biophys Acta 1490: 259-268, 2000.
64. Whitelock JM, Murdoch AD, Iozzo RV, Underwood PA. The degradation of human endothelial cell-derived perlecan and release of bound basic fibroblast growth factor by stromelysin, collagenase, plasmin, and heparanases. J Biol Chem 271: 10079-10086, 1996.
65. Wynn TA, Ramalingam TR. Mechanisms of fibrosis: therapeutic translation for fibrotic disease. Nat Med 18: 1028-1040, 2012.
66. Zachary I, Mathur A, Yla-Herttuala S, Martin J. Vascular protection: a novel nonangiogenic cardiovascular role for vascular endothelial growth factor. Arterioscler Thromb Vasc Biol 20: 1512-1520, 2000.
67. Zaruba MM, Theiss HD, Vallaster M, Mehl U, Brunner S, David R, Fischer R, Krieg L, Hirsch E, Huber B, Nathan P, Israel L, Imhof A, Herbach N, Assmann G, Wanke R, Mueller-Hoecker J, Steinbeck G, Franz WM. Synergy between CD26/DPP-IV inhibition and G-CSF improves cardiac function after acute myocardial infarction. Cell Stem Cell 4: 313-323, 2009.
68. Zimmermann O. Mesenchymal stem cells and cardiac regeneration: a sophisticated approach depends on trophic effects-what's left over? Focus on "Activation of Toll-like receptor 3 amplifies mesenchymal stem cell trophic factors and enhances therapeutic potency". Am J Physiol Cell Physiol 303: C1004-C1005, 2012.
69. Zisa D, Shabbir A, Mastri M, Suzuki G, Lee T. Intramuscular VEGF repairs the failing heart: role of host-derived growth factors and mobilization of progenitor cells. Am J Physiol Regul Integr Comp Physiol 297: R1503-R1515, 2009.
70. Zisa D, Shabbir A, Mastri M, Taylor T, Aleksic I, McDaniel M, Suzuki G, Lee T. Intramuscular VEGF activates an SDF1-dependent progenitor cell cascade and an SDF1-independent muscle paracrine cascade for cardiac repair. Am J Physiol Heart Circ Physiol 301: H2422-H2432, 2011.
71. Zisa D, Shabbir A, Suzuki G, Lee T. Vascular endothelial growth factor (VEGF) as a key therapeutic trophic factor in bone marrow mesenchymal stem cell-mediated cardiac repair. Biochem Biophys Res Commun 390: 834-838, 2009.