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Open Access 01-03-2018

Protein tyrosine phosphatases in cardiac physiology and pathophysiology

Authors: Fallou Wade, Karim Belhaj, Coralie Poizat

Published in: Heart Failure Reviews | Issue 2/2018

Abstract

More than any other organ, the heart is particularly sensitive to gene expression deregulation, often leading in the long run to impaired contractile performances and excessive fibrosis deposition progressing to heart failure. Recent investigations provide evidences that the protein phosphatases (PPs), as their counterpart protein kinases, are important regulators of cardiac physiology and development. Two main groups, the protein serine/threonine phosphatases and the protein tyrosine phosphatases (PTPs), constitute the PPs family. Here, we provide an overview of the role of PTP subfamily in the development of the heart and in cardiac pathophysiology. Based on recent in silico studies, we highlight the importance of PTPs as therapeutic targets for the development of new drugs to restore PTPs signaling in the early and late events of heart failure.

Oudit GY, Kassiri Z, Zhou J, Liu QC, Liu PP, Backx PH, Dawood F, Crackower MA, Scholey JW, Penninger JM (2008) Loss of PTEN attenuates the development of pathological hypertrophy and heart failure in response to biomechanical stress. Cardiovasc Res 78(3):505–514. https://doi.org/10.1093/cvr/cvn041 PubMedCrossRef

Shen YH, Zhang L, Gan Y, Wang X, Wang J, LeMaire SA, Coselli JS, Wang XL (2006) Up-regulation of PTEN (phosphatase and tensin homolog deleted on chromosome ten) mediates p38 MAPK stress signal-induced inhibition of insulin signaling. A cross-talk between stress signaling and insulin signaling in resistin-treated human endothelial cells. J Biol Chem 281(12):7727–7736. https://doi.org/10.1074/jbc.M511105200 PubMedCrossRef

Schramm C, Fine DM, Edwards MA, Reeb AN, Krenz M (2012) The PTPN11 loss-of-function mutation Q510E-Shp2 causes hypertrophic cardiomyopathy by dysregulating mTOR signaling. Am J Phys Heart Circ Phys 302(1):H231–H243. https://doi.org/10.1152/ajpheart.00665.2011

Wade F, Quijada P, Al-Haffar KM et al (2015) Deletion of low molecular weight protein tyrosine phosphatase (Acp1) protects against stress-induced cardiomyopathy. J Pathol 237(4):482–494. https://doi.org/10.1002/path.4594 PubMedPubMedCentralCrossRef

Wang Y (2007) Mitogen-activated protein kinases in heart development and diseases. Circulation 116(12):1413–1423. https://doi.org/10.1161/CIRCULATIONAHA.106.679589 PubMedCrossRef

Swaminathan PD, Purohit A, Hund TJ, Anderson ME (2012) Calmodulin-dependent protein kinase II: linking heart failure and arrhythmias. Circ Res 110(12):1661–1677. https://doi.org/10.1161/CIRCRESAHA.111.243956 PubMedPubMedCentralCrossRef

Dhalla NS, Muller AL (2010) Protein kinases as drug development targets for heart disease therapy. Pharmaceuticals 3(7):2111–2145. https://doi.org/10.3390/ph3072111 PubMedPubMedCentralCrossRef

Nicolaou P, Kranias EG (2009) Role of PP1 in the regulation of Ca cycling in cardiac physiology and pathophysiology. Front Biosci (Landmark Ed) 14:3571–3585CrossRef

Heijman J, Dewenter M, El-Armouche A, Dobrev D (2013) Function and regulation of serine/threonine phosphatases in the healthy and diseased heart. J Mol Cell Cardiol 64:90–98. https://doi.org/10.1016/j.yjmcc.2013.09.006 PubMedCrossRef

10.

Alonso A, Sasin J, Bottini N, Friedberg I, Friedberg I, Osterman A, Godzik A, Hunter T, Dixon J, Mustelin T (2004) Protein tyrosine phosphatases in the human genome. Cell 117(6):699–711. https://doi.org/10.1016/j.cell.2004.05.018 PubMedCrossRef

11.

Tonks NK (2013) Protein tyrosine phosphatases--from housekeeping enzymes to master regulators of signal transduction. FEBS J 280(2):346–378. https://doi.org/10.1111/febs.12077 PubMedPubMedCentralCrossRef

12.

Sugano Y, Lai NC, Gao MH, Firth AL, Yuan JXJ, Lew WYW, Hammond HK (2011) Activated expression of cardiac adenylyl cyclase 6 reduces dilation and dysfunction of the pressure-overloaded heart. Biochem Biophys Res Commun 405(3):349–355. https://doi.org/10.1016/j.bbrc.2010.12.113 PubMedCrossRef

13.

Qian J, Vafiadaki E, Florea SM, Singh VP, Song W, Lam CK, Wang Y, Yuan Q, Pritchard TJ, Cai W, Haghighi K, Rodriguez P, Wang HS, Sanoudou D, Fan GC, Kranias EG (2011) Small heat shock protein 20 interacts with protein phosphatase-1 and enhances sarcoplasmic reticulum calcium cycling. Circ Res 108(12):1429–1438. https://doi.org/10.1161/CIRCRESAHA.110.237644 PubMedPubMedCentralCrossRef

14.

Oh JG, Kim J, Jang SP, Nguen M, Yang DK, Jeong D, Park ZY, Park SG, Hajjar RJ, Park WJ (2013) Decoy peptides targeted to protein phosphatase 1 inhibit dephosphorylation of phospholamban in cardiomyocytes. J Mol Cell Cardiol 56:63–71. https://doi.org/10.1016/j.yjmcc.2012.12.005 PubMedCrossRef

15.

Fan WJ, van Vuuren D, Genade S et al (2010) Kinases and phosphatases in ischaemic preconditioning: a re-evaluation. Basic Res Cardiol 105(4):495–511. https://doi.org/10.1007/s00395-010-0086-3 PubMedCrossRef

16.

Wittkopper K, Dobrev D, Eschenhagen T, El-armouche A (2011) Phosphatase-1 inhibitor-1 in physiological and pathological beta-adrenoceptor signalling. Cardiovasc Res 91(3):392–401. https://doi.org/10.1093/cvr/cvr058 PubMedCrossRef

17.

Cohen P (2002) The origins of protein phosphorylation. Nat Cell Biol 4(5):E127–E130. https://doi.org/10.1038/ncb0502-e127 PubMedCrossRef

18.

Marin TM, Keith K, Davies B, Conner DA, Guha P, Kalaitzidis D, Wu X, Lauriol J, Wang B, Bauer M, Bronson R, Franchini KG, Neel BG, Kontaridis MI (2011) Rapamycin reverses hypertrophic cardiomyopathy in a mouse model of LEOPARD syndrome-associated PTPN11 mutation. J Clin Invest 121(3):1026–1043. https://doi.org/10.1172/JCI44972 PubMedPubMedCentralCrossRef

19.

Tonks NK (2006) Protein tyrosine phosphatases: from genes, to function, to disease. Nat Rev Mol Cell Biol 7(11):833–846. https://doi.org/10.1038/nrm2039 PubMedCrossRef

20.

Sacco F, Perfetto L, Castagnoli L, Cesareni G (2012) The human phosphatase interactome: an intricate family portrait. FEBS Lett 586(17):2732–2739. https://doi.org/10.1016/j.febslet.2012.05.008 PubMedPubMedCentralCrossRef

21.

Stoker AW (2005) Protein tyrosine phosphatases and signalling. J Endocrinol 185(1):19–33. https://doi.org/10.1677/joe.1.06069 PubMedCrossRef

22.

Kappert K, Peters KG, Bohmer FD et al (2005) Tyrosine phosphatases in vessel wall signaling. Cardiovasc Res 65(3):587–598. https://doi.org/10.1016/j.cardiores.2004.08.016 PubMedCrossRef

23.

Senis YA (2013) Protein-tyrosine phosphatases: a new frontier in platelet signal transduction. J Thromb Haemost: JTH 11(10):1800–1813. https://doi.org/10.1111/jth.12359 PubMed

24.

Raugei G, Ramponi G, Chiarugi P (2002) Low molecular weight protein tyrosine phosphatases: small, but smart. Cell Mol Life Sci: CMLS 59(6):941–949. https://doi.org/10.1007/s00018-002-8481-z PubMedCrossRef

25.

Paul S, Lombroso PJ (2003) Receptor and nonreceptor protein tyrosine phosphatases in the nervous system. Cell Mol Life Sci: CMLS 60(11):2465–2482. https://doi.org/10.1007/s00018-003-3123-7 PubMedCrossRef

26.

Boutros R, Lobjois V, Ducommun B (2007) CDC25 phosphatases in cancer cells: key players? Good targets? Nat Rev Cancer 7(7):495–507. https://doi.org/10.1038/nrc2169 PubMedCrossRef

27.

Karisch R, Fernandez M, Taylor P, Virtanen C, St-Germain JR, Jin LL, Harris IS, Mori J, Mak TW, Senis YA, Östman A, Moran MF, Neel BG (2011) Global proteomic assessment of the classical protein-tyrosine phosphatome and “Redoxome”. Cell 146(5):826–840. https://doi.org/10.1016/j.cell.2011.07.020 PubMedPubMedCentralCrossRef

28.

Graves JD, Krebs EG (1999) Protein phosphorylation and signal transduction. Pharmacol Ther 82(2-3):111–121. https://doi.org/10.1016/S0163-7258(98)00056-4 PubMedCrossRef

29.

Ostman A, Hellberg C, Bohmer FD (2006) Protein-tyrosine phosphatases and cancer. Nat Rev Cancer 6(4):307–320. https://doi.org/10.1038/nrc1837 PubMedCrossRef

30.

Koretzky GA, Picus J, Thomas ML, Weiss A (1990) Tyrosine phosphatase CD45 is essential for coupling T-cell antigen receptor to the phosphatidyl inositol pathway. Nature 346(6279):66–68. https://doi.org/10.1038/346066a0 PubMedCrossRef

31.

Ostergaard HL, Shackelford DA, Hurley TR, Johnson P, Hyman R, Sefton BM, Trowbridge IS (1989) Expression of CD45 alters phosphorylation of the lck-encoded tyrosine protein kinase in murine lymphoma T-cell lines. Proc Natl Acad Sci U S A 86(22):8959–8963. https://doi.org/10.1073/pnas.86.22.8959 PubMedPubMedCentralCrossRef

32.

Thomas ML (1999) The regulation of antigen-receptor signaling by protein tyrosine phosphatases: a hole in the story. Curr Opin Immunol 11(3):270–276. https://doi.org/10.1016/S0952-7915(99)80044-2 PubMedCrossRef

33.

Hanafusa H, Torii S, Yasunaga T, Matsumoto K, Nishida E (2004) Shp2, an SH2-containing protein-tyrosine phosphatase, positively regulates receptor tyrosine kinase signaling by dephosphorylating and inactivating the inhibitor Sprouty. J Biol Chem 279(22):22992–22995. https://doi.org/10.1074/jbc.M312498200 PubMedCrossRef

34.

Mustelin T, Alonso A, Bottini N, Huynh H, Rahmouni S, Nika K, Louis-dit-Sully C, Tautz L, Togo SH, Bruckner S, Mena-Duran AV, al-Khouri AM (2004) Protein tyrosine phosphatases in T cell physiology. Mol Immunol 41(6-7):687–700. https://doi.org/10.1016/j.molimm.2004.04.015 PubMedCrossRef

35.

Lauriol J, Jaffre F, Kontaridis MI (2015) The role of the protein tyrosine phosphatase SHP2 in cardiac development and disease. Semin Cell Dev Biol 37:73–81. https://doi.org/10.1016/j.semcdb.2014.09.013 PubMedCrossRef

36.

Lee H, Yi JS, Lawan A, Min K, Bennett AM (2015) Mining the function of protein tyrosine phosphatases in health and disease. Semin Cell Dev Biol 37:66–72. https://doi.org/10.1016/j.semcdb.2014.09.021 PubMedCrossRef

37.

Belin de Chantemele EJ, Muta K, Mintz J, Tremblay ML, Marrero MB, Fulton DJ, Stepp DW (2009) Protein tyrosine phosphatase 1B, a major regulator of leptin-mediated control of cardiovascular function. Circulation 120(9):753–763. https://doi.org/10.1161/CIRCULATIONAHA.109.853077 PubMedCrossRef

38.

Gomez E, Vercauteren M, Kurtz B, Ouvrard-Pascaud A, Mulder P, Henry JP, Besnier M, Waget A, Hooft van Huijsduijnen R, Tremblay ML, Burcelin R, Thuillez C, Richard V (2012) Reduction of heart failure by pharmacological inhibition or gene deletion of protein tyrosine phosphatase 1B. J Mol Cell Cardiol 52(6):1257–1264. https://doi.org/10.1016/j.yjmcc.2012.03.003 PubMedCrossRef

39.

Thiebaut PA, Besnier M, Gomez E, Richard V (2016) Role of protein tyrosine phosphatase 1B in cardiovascular diseases. J Mol Cell Cardiol 101:50–57. https://doi.org/10.1016/j.yjmcc.2016.09.002 PubMedCrossRef

40.

Gogiraju R, Schroeter MR, Bochenek ML, Hubert A, Münzel T, Hasenfuss G, Schäfer K (2016) Endothelial deletion of protein tyrosine phosphatase-1B protects against pressure overload-induced heart failure in mice. Cardiovasc Res 111(3):204–216. https://doi.org/10.1093/cvr/cvw101 PubMedCrossRef

41.

Besnier M, Galaup A, Nicol L, Henry JP, Coquerel D, Gueret A, Mulder P, Brakenhielm E, Thuillez C, Germain S, Richard V, Ouvrard-Pascaud A (2014) Enhanced angiogenesis and increased cardiac perfusion after myocardial infarction in protein tyrosine phosphatase 1B-deficient mice. FASEB J: Off Publ Fed Am Soc Exp Biol 28(8):3351–3361. https://doi.org/10.1096/fj.13-245753 CrossRef

42.

Langdon YG, Goetz SC, Berg AE, Swanik JT, Conlon FL (2007) SHP-2 is required for the maintenance of cardiac progenitors. Development 134(22):4119–4130. https://doi.org/10.1242/dev.009290 PubMedPubMedCentralCrossRef

43.

Uhlen P, Burch PM, Zito CI et al (2006) Gain-of-function/Noonan syndrome SHP-2/Ptpn11 mutants enhance calcium oscillations and impair NFAT signaling. Proc Natl Acad Sci U S A 103(7):2160–2165. https://doi.org/10.1073/pnas.0510876103 PubMedPubMedCentralCrossRef

44.

Kontaridis MI, Yang W, Bence KK, Cullen D, Wang B, Bodyak N, Ke Q, Hinek A, Kang PM, Liao R, Neel BG (2008) Deletion of Ptpn11 (Shp2) in cardiomyocytes causes dilated cardiomyopathy via effects on the extracellular signal-regulated kinase/mitogen-activated protein kinase and RhoA signaling pathways. Circulation 117(11):1423–1435. https://doi.org/10.1161/CIRCULATIONAHA.107.728865 PubMedPubMedCentralCrossRef

45.

Nakamura T, Colbert M, Krenz M, Molkentin JD, Hahn HS, Dorn GW II, Robbins J (2007) Mediating ERK 1/2 signaling rescues congenital heart defects in a mouse model of Noonan syndrome. J Clin Invest 117(8):2123–2132. https://doi.org/10.1172/JCI30756 PubMedPubMedCentralCrossRef

46.

Princen F, Bard E, Sheikh F, Zhang SS, Wang J, Zago WM, Wu D, Trelles RD, Bailly-Maitre B, Kahn CR, Chen Y, Reed JC, Tong GG, Mercola M, Chen J, Feng GS (2009) Deletion of Shp2 tyrosine phosphatase in muscle leads to dilated cardiomyopathy, insulin resistance, and premature death. Mol Cell Biol 29(2):378–388. https://doi.org/10.1128/MCB.01661-08 PubMedCrossRef

47.

Bonetti M, Paardekooper Overman J, Tessadori F, Noël E, Bakkers J, den Hertog J (2014) Noonan and LEOPARD syndrome Shp2 variants induce heart displacement defects in zebrafish. Development 141(9):1961–1970. https://doi.org/10.1242/dev.106310 PubMedCrossRef

48.

Lauriol J, Cabrera JR, Roy A, Keith K, Hough SM, Damilano F, Wang B, Segarra GC, Flessa ME, Miller LE, Das S, Bronson R, Lee KH, Kontaridis MI (2016) Developmental SHP2 dysfunction underlies cardiac hypertrophy in Noonan syndrome with multiple lentigines. J Clin Invest 126(8):2989–3005. https://doi.org/10.1172/JCI80396 PubMedPubMedCentralCrossRef

49.

Frangioni JV, Beahm PH, Shifrin V, Jost CA, Neel BG (1992) The nontransmembrane tyrosine phosphatase PTP-1B localizes to the endoplasmic reticulum via its 35 amino acid C-terminal sequence. Cell 68(3):545–560. https://doi.org/10.1016/0092-8674(92)90190-N PubMedCrossRef

50.

Salmeen A, Andersen JN, Myers MP, Tonks NK, Barford D (2000) Molecular basis for the dephosphorylation of the activation segment of the insulin receptor by protein tyrosine phosphatase 1B. Mol Cell 6(6):1401–1412. https://doi.org/10.1016/S1097-2765(00)00137-4 PubMedCrossRef

51.

Egawa K, Maegawa H, Shimizu S, Morino K, Nishio Y, Bryer-Ash M, Cheung AT, Kolls JK, Kikkawa R, Kashiwagi A (2001) Protein-tyrosine phosphatase-1B negatively regulates insulin signaling in l6 myocytes and Fao hepatoma cells. J Biol Chem 276(13):10207–10211. https://doi.org/10.1074/jbc.M009489200 PubMedCrossRef

52.

Panzhinskiy E, Ren J, Nair S (2013) Protein tyrosine phosphatase 1B and insulin resistance: role of endoplasmic reticulum stress/reactive oxygen species/nuclear factor kappa B axis. PLoS One 8(10):e77228. https://doi.org/10.1371/journal.pone.0077228 PubMedPubMedCentralCrossRef

53.

Feizi S (2009) Protein tyrosine phosphatase-1B (PTP1B) regulates EGF-induced stimulation of corneal endothelial cell proliferation. J Ophthalmic Vis Res 4(2):127–128PubMedPubMedCentral

54.

Cheng A, Dube N, Gu F et al (2002) Coordinated action of protein tyrosine phosphatases in insulin signal transduction. Eur J Biochem 269(4):1050–1059. https://doi.org/10.1046/j.0014-2956.2002.02756.x PubMedCrossRef

55.

Cho H (2013) Protein tyrosine phosphatase 1B (PTP1B) and obesity. Vitam Horm 91:405–424. https://doi.org/10.1016/B978-0-12-407766-9.00017-1 PubMedCrossRef

56.

Elchebly M, Payette P, Michaliszyn E, Cromlish W, Collins S, Loy AL, Normandin D, Cheng A, Himms-Hagen J, Chan CC, Ramachandran C, Gresser MJ, Tremblay ML, Kennedy BP (1999) Increased insulin sensitivity and obesity resistance in mice lacking the protein tyrosine phosphatase-1B gene. Science 283(5407):1544–1548. https://doi.org/10.1126/science.283.5407.1544 PubMedCrossRef

57.

Klaman LD, Boss O, Peroni OD, Kim JK, Martino JL, Zabolotny JM, Moghal N, Lubkin M, Kim YB, Sharpe AH, Stricker-Krongrad A, Shulman GI, Neel BG, Kahn BB (2000) Increased energy expenditure, decreased adiposity, and tissue-specific insulin sensitivity in protein-tyrosine phosphatase 1B-deficient mice. Mol Cell Biol 20(15):5479–5489. https://doi.org/10.1128/MCB.20.15.5479-5489.2000 PubMedPubMedCentralCrossRef

58.

Rahmouni K, Correia ML, Haynes WG et al (2005) Obesity-associated hypertension: new insights into mechanisms. Hypertension 45(1):9–14. https://doi.org/10.1161/01.HYP.0000151325.83008.b4 PubMedCrossRef

59.

Kalil GZ, Haynes WG (2012) Sympathetic nervous system in obesity-related hypertension: mechanisms and clinical implications. Hypertens Res: Off J Japn Soc Hypertens 35(1):4–16. https://doi.org/10.1038/hr.2011.173 CrossRef

60.

Fang CX, Doser TA, Yang X, Sreejayan N, Ren J (2006) Metallothionein antagonizes aging-induced cardiac contractile dysfunction: role of PTP1B, insulin receptor tyrosine phosphorylation and Akt. Aging Cell 5(2):177–185. https://doi.org/10.1111/j.1474-9726.2006.00201.x PubMedCrossRef

61.

Dong F, Fang CX, Yang X, Zhang X, Lopez FL, Ren J (2006) Cardiac overexpression of catalase rescues cardiac contractile dysfunction induced by insulin resistance: role of oxidative stress, protein carbonyl formation and insulin sensitivity. Diabetologia 49(6):1421–1433. https://doi.org/10.1007/s00125-006-0230-7 PubMedCrossRef

62.

Herren DJ, Norman JB, Anderson R et al (2015) Deletion of protein tyrosine phosphatase 1B (PTP1B) enhances endothelial cyclooxygenase 2 expression and protects mice from type 1 diabetes-induced endothelial dysfunction. PLoS One 10(5):e0126866. https://doi.org/10.1371/journal.pone.0126866 PubMedCrossRef

63.

Cui C, Merritt R, Fu L, Pan Z (2017) Targeting calcium signaling in cancer therapy. Acta Pharm Sin B 7(1):3–17. https://doi.org/10.1016/j.apsb.2016.11.001 PubMedCrossRef

64.

Neel BG, Gu H, Pao L (2003) The 'Shp'ing news: SH2 domain-containing tyrosine phosphatases in cell signaling. Trends Biochem Sci 28(6):284–293. https://doi.org/10.1016/S0968-0004(03)00091-4 PubMedCrossRef

65.

Ishida H, Kogaki S, Narita J, Ichimori H, Nawa N, Okada Y, Takahashi K, Ozono K (2011) LEOPARD-type SHP2 mutant Gln510Glu attenuates cardiomyocyte differentiation and promotes cardiac hypertrophy via dysregulation of Akt/GSK-3beta/beta-catenin signaling. Am J Phys Heart Circ Phys 301(4):H1531–H1539. https://doi.org/10.1152/ajpheart.00216.2011

66.

Chan RJ, Li Y, Hass MN, Walter A, Voorhorst CS, Shelley WC, Yang Z, Orschell CM, Yoder MC (2006) Shp-2 heterozygous hematopoietic stem cells have deficient repopulating ability due to diminished self-renewal. Exp Hematol 34(9):1230–1239. https://doi.org/10.1016/j.exphem.2006.04.017 PubMedCrossRef

67.

Yang W, Klaman LD, Chen B, Araki T, Harada H, Thomas SM, George EL, Neel BG (2006) An Shp2/SFK/Ras/Erk signaling pathway controls trophoblast stem cell survival. Dev Cell 10(3):317–327. https://doi.org/10.1016/j.devcel.2006.01.002 PubMedCrossRef

68.

Noonan J, O'Connor W (1996) Noonan syndrome: a clinical description emphasizing the cardiac findings. Acta Paediatr Jpn: Overseas Ed 38(1):76–83. https://doi.org/10.1111/j.1442-200X.1996.tb03443.x CrossRef

69.

Tartaglia M, Mehler EL, Goldberg R, Zampino G, Brunner HG, Kremer H, van der Burgt I, Crosby AH, Ion A, Jeffery S, Kalidas K, Patton MA, Kucherlapati RS, Gelb BD (2001) Mutations in PTPN11, encoding the protein tyrosine phosphatase SHP-2, cause Noonan syndrome. Nat Genet 29(4):465–468. https://doi.org/10.1038/ng772 PubMedCrossRef

70.

Lauriol J, Kontaridis MI (2011) PTPN11-associated mutations in the heart: has LEOPARD changed its RASpots? Trends Cardiovasc Med 21(4):97–104. https://doi.org/10.1016/j.tcm.2012.03.006 PubMedPubMedCentralCrossRef

71.

Tafazoli A, Eshraghi P, Koleti ZK, Abbaszadegan M (2017) Noonan syndrome—a new survey. Arch Med Sci: AMS 13(1):215–222. https://doi.org/10.5114/aoms.2017.64720 PubMedCrossRef

72.

Keilhack H, David FS, McGregor M, Cantley LC, Neel BG (2005) Diverse biochemical properties of Shp2 mutants. Implications for disease phenotypes. J Biol Chem 280(35):30984–30993. https://doi.org/10.1074/jbc.M504699200 PubMedCrossRef

73.

Kontaridis MI, Swanson KD, David FS, Barford D, Neel BG (2006) PTPN11 (Shp2) mutations in LEOPARD syndrome have dominant negative, not activating, effects. J Biol Chem 281(10):6785–6792. https://doi.org/10.1074/jbc.M513068200 PubMedCrossRef

74.

Yu ZH, Zhang RY, Walls CD, Chen L, Zhang S, Wu L, Liu S, Zhang ZY (2014) Molecular basis of gain-of-function LEOPARD syndrome-associated SHP2 mutations. Biochemistry 53(25):4136–4151. https://doi.org/10.1021/bi5002695 PubMedPubMedCentralCrossRef

75.

Xu M, Jin Y, Song Q, Wu J, Philbrick MJ, Cully BL, An X, Guo L, Gao F, Li J (2011) The endothelium-dependent effect of RTEF-1 in pressure overload cardiac hypertrophy: role of VEGF-B. Cardiovasc Res 90(2):325–334. https://doi.org/10.1093/cvr/cvq400 PubMedCrossRef

76.

Bottini N, Bottini E, Gloria-Bottini F, Mustelin T (2002) Low-molecular-weight protein tyrosine phosphatase and human disease: in search of biochemical mechanisms. Arch Immunol Ther Exp 50(2):95–104

77.

Chernoff J, Li HC (1985) A major phosphotyrosyl-protein phosphatase from bovine heart is associated with a low-molecular-weight acid phosphatase. Arch Biochem Biophys 240(1):135–145. https://doi.org/10.1016/0003-9861(85)90016-5 PubMedCrossRef

78.

Magherini F, Giannoni E, Raugei G, Cirri P, Paoli P, Modesti A, Camici G, Ramponi G (1998) Cloning of murine low molecular weight phosphotyrosine protein phosphatase cDNA: identification of a new isoform. FEBS Lett 437(3):263–266. https://doi.org/10.1016/S0014-5793(98)01241-1 PubMedCrossRef

79.

Lazaruk KD, Dissing J, Sensabaugh GF (1993) Exon structure at the human ACP1 locus supports alternative splicing model for f and s isozyme generation. Biochem Biophys Res Commun 196(1):440–446. https://doi.org/10.1006/bbrc.1993.2269 PubMedCrossRef

80.

Cirri P, Fiaschi T, Chiarugi P, Camici G, Manao G, Raugei G, Ramponi G (1996) The molecular basis of the differing kinetic behavior of the two low molecular mass phosphotyrosine protein phosphatase isoforms. J Biol Chem 271(5):2604–2607. https://doi.org/10.1074/jbc.271.5.2604 PubMedCrossRef

81.

Pandey SK, Yu XX, Watts LM, et al. 2007 Reduction of low-molecular-weight protein tyrosine phosphatase expression improves hyperglycemia and insulin sensitivity in obese mice. J Biol Chem

82.

Ramponi G, Manao G, Camici G, Cappugi G, Ruggiero M, Bottaro DP (1989) The 18 kDa cytosolic acid phosphatase from bovine live has phosphotyrosine phosphatase activity on the autophosphorylated epidermal growth factor receptor. FEBS Lett 250(2):469–473. https://doi.org/10.1016/0014-5793(89)80778-1 PubMedCrossRef

83.

Hoekstra E, Peppelenbosch MP, Fuhler GM (1826) The role of protein tyrosine phosphatases in colorectal cancer. Biochim Biophys Acta 2012:179–188

84.

Xing K, Raza A, Lofgren S et al (2007) Low molecular weight protein tyrosine phosphatase (LMW-PTP) and its possible physiological functions of redox signaling in the eye lens. Biochim Biophys Acta 1774(5):545–555. https://doi.org/10.1016/j.bbapap.2007.03.001 PubMedPubMedCentralCrossRef

85.

Kikawa KD, Vidale DR, Van Etten RL, Kinch MS (2002) Regulation of the EphA2 kinase by the low molecular weight tyrosine phosphatase induces transformation. J Biol Chem 277(42):39274–39279. https://doi.org/10.1074/jbc.M207127200 PubMedCrossRef

86.

Park EK, Warner N, Mood K, Pawson T, Daar IO (2002) Low-molecular-weight protein tyrosine phosphatase is a positive component of the fibroblast growth factor receptor signaling pathway. Mol Cell Biol 22(10):3404–3414. https://doi.org/10.1128/MCB.22.10.3404-3414.2002 PubMedPubMedCentralCrossRef

87.

Dissing J (1993) Human “red cell” acid phosphatase (ACP1) genetic, catalytic and molecular properties. PhD Thesis, Copenhagen University, Copenhagen, Denmark

88.

Bottini N, MacMurray J, Peters W, Rostamkhani M, Comings DE (2002) Association of the acid phosphatase (ACP1) gene with triglyceride levels in obese women. Mol Genet Metab 77(3):226–229. https://doi.org/10.1016/S1096-7192(02)00120-8 PubMedCrossRef

89.

Shu YH, Hartiala J, Xiang AH, Trigo E, Lawrence JM, Allayee H, Buchanan TA, Bottini N, Watanabe RM (2009) Evidence for sex-specific associations between variation in acid phosphatase locus 1 (ACP1) and insulin sensitivity in Mexican-Americans. J Clin Endocrinol Metab 94(10):4094–4102. https://doi.org/10.1210/jc.2008-2751 PubMedPubMedCentralCrossRef

90.

Banci M, Saccucci P, D’Annibale F et al (2009) ACP1 genetic polymorphism and coronary artery disease: an association study. Cardiology 113(4):236–242. https://doi.org/10.1159/000203405 PubMedCrossRef

91.

Bottini E, Gloria-Bottini F, Borgiani P (1995) ACP1 and human adaptability. 1. Association with common diseases: a case-control study. Hum Genet 96(6):629–637. https://doi.org/10.1007/BF00210290 PubMedCrossRef

92.

Huyer G, Liu S, Kelly J, Moffat J, Payette P, Kennedy B, Tsaprailis G, Gresser MJ, Ramachandran C (1997) Mechanism of inhibition of protein-tyrosine phosphatases by vanadate and pervanadate. J Biol Chem 272(2):843–851. https://doi.org/10.1074/jbc.272.2.843 PubMedCrossRef

93.

Bhuiyan MS, Takada Y, Shioda N, Moriguchi S, Kasahara J, Fukunaga K (2008) Cardioprotective effect of vanadyl sulfate on ischemia/reperfusion-induced injury in rat heart in vivo is mediated by activation of protein kinase B and induction of FLICE-inhibitory protein. Cardiovasc Ther 26(1):10–23. https://doi.org/10.1111/j.1527-3466.2008.00039.x PubMed

94.

Goldfine AB, Patti ME, Zuberi L, Goldstein BJ, LeBlanc R, Landaker EJ, Jiang ZY, Willsky GR, Kahn CR (2000) Metabolic effects of vanadyl sulfate in humans with non-insulin-dependent diabetes mellitus: in vivo and in vitro studies. Metab Clin Exp 49(3):400–410. https://doi.org/10.1016/S0026-0495(00)90418-9 PubMedCrossRef

95.

Vercauteren M, Remy E, Devaux C, Dautreaux B, Henry JP, Bauer F, Mulder P, Hooft van Huijsduijnen R, Bombrun A, Thuillez C, Richard V (2006) Improvement of peripheral endothelial dysfunction by protein tyrosine phosphatase inhibitors in heart failure. Circulation 114(23):2498–2507. https://doi.org/10.1161/CIRCULATIONAHA.106.630129 PubMedCrossRef

96.

Schramm C, Edwards MA, Krenz M (2013) New approaches to prevent LEOPARD syndrome-associated cardiac hypertrophy by specifically targeting Shp2-dependent signaling. J Biol Chem 288(25):18335–18344. https://doi.org/10.1074/jbc.M113.483800 PubMedPubMedCentralCrossRef

97.

Forghieri M, Laggner C, Paoli P, Langer T, Manao G, Camici G, Bondioli L, Prati F, Costantino L (2009) Synthesis, activity and molecular modeling of a new series of chromones as low molecular weight protein tyrosine phosphatase inhibitors. Bioorg Med Chem 17(7):2658–2672. https://doi.org/10.1016/j.bmc.2009.02.060 PubMedCrossRef

98.

Stanford SM, Aleshin AE, Zhang V, et al. 2017 Diabetes reversal by inhibition of the low-molecular-weight tyrosine phosphatase. Nat Chem Biol

99.

Lantz KA, Hart SG, Planey SL et al (2010) Inhibition of PTP1B by trodusquemine (MSI-1436) causes fat-specific weight loss in diet-induced obese mice. Obesity 18(8):1516–1523. https://doi.org/10.1038/oby.2009.444 PubMedCrossRef

100.

He R, Wang J, Yu ZH, et al. (2016) Inhibition of low molecular weight protein tyrosine phosphatase by an induced-fit mechanism. J Med Chem

101.

Hellmuth K, Grosskopf S, Lum CT, Wurtele M, Roder N, von Kries JP, Rosario M, Rademann J, Birchmeier W (2008) Specific inhibitors of the protein tyrosine phosphatase Shp2 identified by high-throughput docking. Proc Natl Acad Sci U S A 105(20):7275–7280. https://doi.org/10.1073/pnas.0710468105 PubMedPubMedCentralCrossRef

102.

Yu B, Liu W, Yu WM, Loh ML, Alter S, Guvench O, MacKerell AD, Tang LD, Qu CK (2013) Targeting protein tyrosine phosphatase SHP2 for the treatment of PTPN11-associated malignancies. Mol Cancer Ther 12(9):1738–1748. https://doi.org/10.1158/1535-7163.MCT-13-0049-T PubMedPubMedCentralCrossRef

103.

Chen L, Sung SS, Yip ML, Lawrence HR, Ren Y, Guida WC, Sebti SM, Lawrence NJ, Wu J (2006) Discovery of a novel shp2 protein tyrosine phosphatase inhibitor. Mol Pharmacol 70(2):562–570. https://doi.org/10.1124/mol.106.025536 PubMedCrossRef

104.

Sippl W (2002) Development of biologically active compounds by combining 3D QSAR and structure-based design methods. J Comput Aided Mol Des 16(11):825–830. https://doi.org/10.1023/A:1023888813526 PubMedCrossRef

105.

Yu WM, Guvench O, Mackerell AD et al (2008) Identification of small molecular weight inhibitors of Src homology 2 domain-containing tyrosine phosphatase 2 (SHP-2) via in silico database screening combined with experimental assay. J Med Chem 51(23):7396–7404. https://doi.org/10.1021/jm800229d PubMedPubMedCentralCrossRef

106.

Sobhia ME, Paul S, Shinde R et al (2012) Protein tyrosine phosphatase inhibitors: a patent review (2002–2011). Expert Opin Ther Patents 22(2):125–153. https://doi.org/10.1517/13543776.2012.661414 CrossRef

107.

Hof P, Pluskey S, Dhe-Paganon S, Eck MJ, Shoelson SE (1998) Crystal structure of the tyrosine phosphatase SHP-2. Cell 92(4):441–450. https://doi.org/10.1016/S0092-8674(00)80938-1 PubMedCrossRef

108.

Lee JO, Yang H, Georgescu MM, di Cristofano A, Maehama T, Shi Y, Dixon JE, Pandolfi P, Pavletich NP (1999) Crystal structure of the PTEN tumor suppressor: implications for its phosphoinositide phosphatase activity and membrane association. Cell 99(3):323–334. https://doi.org/10.1016/S0092-8674(00)81663-3 PubMedCrossRef

109.

Wiesmann C, Barr KJ, Kung J, Zhu J, Erlanson DA, Shen W, Fahr BJ, Zhong M, Taylor L, Randal M, McDowell RS, Hansen SK (2004) Allosteric inhibition of protein tyrosine phosphatase 1B. Nat Struct Mol Biol 11(8):730–737. https://doi.org/10.1038/nsmb803 PubMedCrossRef

110.

Scott LM, Chen L, Daniel KG, Brooks WH, Guida WC, Lawrence HR, Sebti SM, Lawrence NJ, Wu J (2011) Shp2 protein tyrosine phosphatase inhibitor activity of estramustine phosphate and its triterpenoid analogs. Bioorg Med Chem Lett 21(2):730–733. https://doi.org/10.1016/j.bmcl.2010.11.117 PubMedCrossRef

111.

Scott LM, Lawrence HR, Sebti SM et al (2010) Targeting protein tyrosine phosphatases for anticancer drug discovery. Curr Pharm Des 16(16):1843–1862. https://doi.org/10.2174/138161210791209027 PubMedPubMedCentralCrossRef

Title: Protein tyrosine phosphatases in cardiac physiology and pathophysiology
Authors: Fallou Wade
Karim Belhaj
Coralie Poizat
Publication date: 01-03-2018
Publisher: Springer US
Published in: Heart Failure Reviews / Issue 2/2018
Print ISSN: 1382-4147
Electronic ISSN: 1573-7322
DOI: https://doi.org/10.1007/s10741-018-9676-1

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