Blockade to pathological remodeling of infarcted heart tissue using a porcupine antagonist

Proceedings of the National Academy of Sciences of the United States of America

Volumn 114, Issue 7, 2017, Pages 1649-1654

  Moon, Jesung ^a   Zhou, Huanyu ^b   Zhang, Li Shu ^b   Tan, Wei ^b   Liu, Ying ^c   Zhang, Shanrong ^b   Morlock, Lorraine K ^a   Bao, Xiaoping ^d   Palecek, Sean P ^d   Feng, Jian Q ^c   Williams, Noelle S ^a   Amatruda, James F ^a,b   Olson, Eric N ^b   Bassel Duby, Rhonda ^b   Lum, Lawrence ^b  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c Texas A and M Health Sciences Center   (United States)

^d Wisconsin Electric Machines and Power Electronics Consortium   (United States)

Author keywords

Adult tissue homeostasis; Extracellular matrix; Heart regeneration; Protein lipidation; Wnt

Indexed keywords

ANTIFIBROTIC AGENT; BETA CATENIN; CARDIOVASCULAR AGENT; COLLAGEN TYPE 1; COLLAGEN TYPE 6; COLLAGEN TYPE 6 ALPHA 1; CONNECTIVE TISSUE GROWTH FACTOR; CYCLINE; DISHEVELLED 2; NONFIBRILLAR COLLAGEN VI; UNCLASSIFIED DRUG; WNT 974; WNT3A PROTEIN; ACYLTRANSFERASE; ENZYME INHIBITOR; MEMBRANE PROTEIN; PORCN PROTEIN, MOUSE;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COLLAGEN SYNTHESIS; CONTROLLED STUDY; CORONARY ARTERY LIGATION; EXTRACELLULAR MATRIX; GENE DELETION; HEART FUNCTION; HEART INFARCTION; HEART MUSCLE FIBROSIS; HEART TISSUE; IN VITRO STUDY; IN VIVO STUDY; LEFT ANTERIOR DESCENDING CORONARY ARTERY; MITOSIS RATE; NONHUMAN; OSSIFICATION; PRIORITY JOURNAL; TISSUE REGENERATION; TRANSCRIPTION INITIATION; WNT SIGNALING PATHWAY; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; CELL CULTURE; CHEMICAL STRUCTURE; CHEMISTRY; DRUG EFFECT; GENE EXPRESSION; GENETICS; HEART ATRIUM REMODELING; HEK293 CELL LINE; HUMAN; METABOLISM; PATHOPHYSIOLOGY; REGENERATION; WNT SIGNALING;

ACYLTRANSFERASES; ANIMALS; ATRIAL REMODELING; CELLS, CULTURED; COLLAGEN TYPE VI; ENZYME INHIBITORS; GENE EXPRESSION; HEK293 CELLS; HUMANS; MEMBRANE PROTEINS; MICE, INBRED C57BL; MOLECULAR STRUCTURE; MYOCARDIAL INFARCTION; REGENERATION; WNT SIGNALING PATHWAY;

EID: 85013083593     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1621346114     Document Type: Article

References (56)

1. Kong P, Christia P, Frangogiannis NG (2014) The pathogenesis of cardiac fibrosis. Cell Mol Life Sci 71(4):549-574.
2. Gourdie RG, Dimmeler S, Kohl P (2016) Novel therapeutic strategies targeting fibroblasts and fibrosis in heart disease. Nat Rev Drug Discov 15(9):620-638.
3. Bartscherer K, Boutros M (2008) Regulation of Wnt protein secretion and its role in gradient formation. EMBO Rep 9(10):977-982.
4. Kadowaki T, Wilder E, Klingensmith J, Zachary K, Perrimon N (1996) The segment polarity gene porcupine encodes a putative multitransmembrane protein involved in Wingless processing. Genes Dev 10(24):3116-3128.
5. Tanaka K, Okabayashi K, Asashima M, Perrimon N, Kadowaki T (2000) The evolutionarily conserved porcupine gene family is involved in the processing of the Wnt family. Eur J Biochem 267(13):4300-4311.
6. Willert K, et al. (2003) Wnt proteins are lipid-modified and can act as stem cell growth factors. Nature 423(6938):448-452.
7. Takada R, et al. (2006) Monounsaturated fatty acid modification of Wnt protein: Its role in Wnt secretion. Dev Cell 11(6):791-801.
8. Chen B, et al. (2009) Small molecule-mediated disruption of Wnt-dependent signaling in tissue regeneration and cancer. Nat Chem Biol 5(2):100-107.
9. Lum L, Chen C (2015) Chemical disruption of Wnt-dependent cell fate decision-making mechanisms in cancer and regenerative medicine. Curr Med Chem 22(35):4091-4103.
10. Juan J, Muraguchi T, Iezza G, Sears RC, McMahon M (2014) Diminished WNT -> β-catenin -> c-MYC signaling is a barrier for malignant progression of BRAFV600E-induced lung tumors. Genes Dev 28(6):561-575.
11. Liu J, et al. (2013) Targeting Wnt-driven cancer through the inhibition of Porcupine by LGK974. Proc Natl Acad Sci USA 110(50):20224-20229.
12. Clevers H (2013) The intestinal crypt, a prototype stem cell compartment. Cell 154(2):274-284.
13. Goldring MB, Marcu KB (2009) Cartilage homeostasis in health and rheumatic diseases. Arthritis Res Ther 11(3):224.
14. Lim X, Tan SH, Yu KL, Lim SB, Nusse R (2016) Axin2 marks quiescent hair follicle bulge stem cells that are maintained by autocrine Wnt/β-catenin signaling. Proc Natl Acad Sci USA 113(11):E1498-E1505.
15. Zhong Z, Ethen NJ, Williams BO (2014) WNT signaling in bone development and homeostasis. Wiley Interdiscip Rev Dev Biol 3(6):489-500.
16. Kabiri Z, et al. (2015) Wnts are dispensable for differentiation and self-renewal of adult murine hematopoietic stem cells. Blood 126(9):1086-1094.
17. Proffitt KD, Virshup DM (2012) Precise regulation of porcupine activity is required for physiological Wnt signaling. J Biol Chem 287(41):34167-34178.
18. Foglia MJ, Poss KD (2016) Building and re-building the heart by cardiomyocyte proliferation. Development 143(5):729-740.
19. Grünberg JR, Hammarstedt A, Hedjazifar S, Smith U (2014) The novel secreted adipokine WNT1-inducible signaling pathway protein 2 (WISP2) is a mesenchymal cell activator of canonical WNT. J Biol Chem 289(10):6899-6907.
20. Kessenbrock K, et al. (2013) A role for matrix metalloproteinases in regulating mammary stem cell function via the Wnt signaling pathway. Cell Stem Cell 13(3):300-313.
21. Si W, et al. (2006) CCN1/Cyr61 is regulated by the canonical Wnt signal and plays an important role in Wnt3A-induced osteoblast differentiation of mesenchymal stem cells. Mol Cell Biol 26(8):2955-2964.
22. Bao MW, et al. (2015) Dickkopf-3 protects against cardiac dysfunction and ventricular remodelling following myocardial infarction. Basic Res Cardiol 110(3):25.
23. Luther DJ, et al. (2012) Absence of type VI collagen paradoxically improves cardiac function, structure, and remodeling after myocardial infarction. Circ Res 110(6):851-856.
24. Bönnemann CG (2011) The collagen VI-related myopathies: Muscle meets its matrix. Nat Rev Neurol 7(7):379-390.
25. Eghbali M (1992) Cardiac fibroblasts: Function, regulation of gene expression, and phenotypic modulation. Basic Res Cardiol 87(Suppl 2):183-189.
26. Pinto AR, et al. (2016) Revisiting cardiac cellular composition. Circ Res 118(3):400-409.
27. Lian X, et al. (2013) Directed cardiomyocyte differentiation from human pluripotent stem cells by modulating Wnt/β-catenin signaling under fully defined conditions. Nat Protoc 8(1):162-175.
28. Bedut S, et al. (2016) High-throughput drug profiling with voltage- and calcium-sensitive fluorescent probes in human iPSC-derived cardiomyocytes. Am J Physiol Heart Circ Physiol 311(1):H44-H53.
29. Fonoudi H, et al. (2015) A universal and robust integrated platform for the scalable production of human cardiomyocytes from pluripotent stem cells. Stem Cells Transl Med 4(12):1482-1494.
30. Matsa E, et al. (2016) Transcriptome profiling of patient-specific human iPSC-cardiomyocytes predicts individual drug safety and efficacy responses in vitro. Cell Stem Cell 19(3):311-325.
31. Riegler J, et al. (2015) Human engineered heart muscles engraft and survive long term in a rodent myocardial infarction model. Circ Res 117(8):720-730.
32. Gao C, Chen YG (2010) Dishevelled: The hub of Wnt signaling. Cell Signal 22(5):717-727.
33. Baudino TA, Carver W, Giles W, Borg TK (2006) Cardiac fibroblasts: Friend or foe? Am J Physiol Heart Circ Physiol 291(3):H1015-H1026.
34. Luo Q, et al. (2004) Connective tissue growth factor (CTGF) is regulated by Wnt and bone morphogenetic proteins signaling in osteoblast differentiation of mesenchymal stem cells. J Biol Chem 279(53):55958-55968.
35. Liehn EA, Postea O, Curaj A, Marx N (2011) Repair after myocardial infarction, between fantasy and reality: The role of chemokines. J Am Coll Cardiol 58(23):2357-2362.
36. Deb A (2014) Cell-cell interaction in the heart via Wnt/β-catenin pathway after cardiac injury. Cardiovasc Res 102(2):214-223.
37. Rucklidge GJ, Milne G, McGaw BA, Milne E, Robins SP (1992) Turnover rates of different collagen types measured by isotope ratio mass spectrometry. Biochim Biophys Acta 1156(1):57-61.
38. Bastokoty D, et al. (May 30, 2016) Temporary, systemic inhibition of the WNT/β-catenin pathway promotes regenerative cardiac repair following myocardial infarct. Cell Stem Cells Regen Med, 10.16966/2472-6990.111.
39. Mohamed TM, et al. (November 10, 2016) Chemical enhancement of in vitro and in vivo direct cardiac reprogramming. Circulation, 10.1161/CIRCULATIONAHA.116.024692.
40. Mizutani M, Wu JC, Nusse R (2016) Fibrosis of the neonatal mouse heart after cryoinjury is accompanied by Wnt signaling activation and epicardial-to-mesenchymal transition. J Am Heart Assoc 5(3):e002457.
41. Shinde AV, Frangogiannis NG (2014) Fibroblasts in myocardial infarction: A role in inflammation and repair. J Mol Cell Cardiol 70:74-82.
42. Saraswati S, et al. (2010) Pyrvinium, a potent small molecule Wnt inhibitor, promotes wound repair and post-MI cardiac remodeling. PLoS One 5(11):e15521.
43. Sasaki T, Hwang H, Nguyen C, Kloner RA, Kahn M (2013) The small molecule Wnt signaling modulator ICG-001 improves contractile function in chronically infarcted rat myocardium. PLoS One 8(9):e75010.
44. Madan B, et al. (2016) Experimental inhibition of porcupine-mediated Wnt O-acylation attenuates kidney fibrosis. Kidney Int 89(5):1062-1074.
45. Brack AS, et al. (2007) Increased Wnt signaling during aging alters muscle stem cell fate and increases fibrosis. Science 317(5839):807-810.
46. Bucholz EM, et al. (2015) Life expectancy and years of potential life lost after acute myocardial infarction by sex and race: A cohort-based study of medicare beneficiaries. J Am Coll Cardiol 66(6):645-655.
47. Zhang LS, Lum L (2016) Delivery of the Porcupine inhibitor WNT974 in mice. Methods Mol Biol 1481:111-117.
48. Dennis G, Jr, et al. (2003) DAVID: Database for annotation, visualization, and integrated discovery. Genome Biol 4(5):3.
49. Doevendans PA, Daemen MJ, de Muinck ED, Smits JF (1998) Cardiovascular pheno-typing in mice. Cardiovasc Res 39(1):34-49.
50. Liu TF, et al. (2012) Ablation of gp78 in liver improves hyperlipidemia and insulin resistance by inhibiting SREBP to decrease lipid biosynthesis. Cell Metab 16(2):213-225.
51. Yoshida Y, et al. (2003) Fbs2 is a new member of the E3 ubiquitin ligase family that recognizes sugar chains. J Biol Chem 278(44):43877-43884.
52. Ma Y, Hendershot LM (2004) Herp is dually regulated by both the endoplasmic reticulum stress-specific branch of the unfolded protein response and a branch that is shared with other cellular stress pathways. J Biol Chem 279(14):13792-13799.
53. Patra D, DeLassus E, Liang G, Sandell LJ (2014) Cartilage-specific ablation of site-1 protease in mice results in the endoplasmic reticulum entrapment of type IIb procollagen and down-regulation of cholesterol and lipid homeostasis. PLoS One 9(8):e105674.
54. Lavoie C, Meerloo T, Lin P, Farquhar MG (2002) Calnuc, an EF-hand Ca(2+)-binding protein, is stored and processed in the Golgi and secreted by the constitutive-like pathway in AtT20 cells. Mol Endocrinol 16(11):2462-2474.
55. Sun S, et al. (2014) Sel1L is indispensable for mammalian endoplasmic reticulum-associated degradation, endoplasmic reticulum homeostasis, and survival. Proc Natl Acad Sci USA 111(5):E582-E591.
56. Doroudgar S, et al. (2015) Hrd1 and ER-associated protein degradation, ERAD, are critical elements of the adaptive ER stress response in cardiac myocytes. Circ Res 117(6):536-546.