HIPPO-integrin-linked kinase cross-talk controls self-sustaining proliferation and survival in pulmonary hypertension

American Journal of Respiratory and Critical Care Medicine

Volumn 194, Issue 7, 2016, Pages 866-877

  Kudryashova, Tatiana V ^a   Goncharov, Dmitry A ^a   Pena, Andressa ^a   Kelly, Neil ^a   Vanderpool, Rebecca ^a   Baust, Jeff ^a   Kobir, Ahasanul ^a   Shufesky, William ^a   Mora, Ana L ^a   Morelli, Adrian E ^a   Zhao, Jing ^a   Ihida Stansbury, Kaori ^b   Chang, Baojun ^a   DeLisser, Horace ^b,c   Tuder, Rubin M ^d   Kawut, Steven M ^b   Silljé, Herman H W ^e   Shapiro, Steven ^a   Zhao, Yutong ^a   Goncharova, Elena A ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d UNIVERSITY OF COLORADO   (United States)

^e UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

Author keywords

HIPPO LATS1; ILK; PAH; Proliferation apoptosis imbalance; Vascular smooth muscle

Indexed keywords

BETA CATENIN; HIPPO KINASE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; INTEGRIN LINKED KINASE; LARGE TUMOR SUPPRESSOR 1 PROTEIN; MAMMALIAN TARGET OF RAPAMYCIN; NOTCH3 RECEPTOR; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG; YES ASSOCIATED PROTEIN;

ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL COUNT; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; DNA SYNTHESIS; ENZYME INACTIVATION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; HUMAN TISSUE; IMMUNOBLOTTING; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; LUNG PARENCHYMA; MOUSE; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PULMONARY ARTERIAL VASCULAR SMOOTH MUSCLE CELL; PULMONARY HYPERTENSION; RAT; SIGNAL TRANSDUCTION; UPREGULATION; VASCULAR REMODELING; VASCULAR SMOOTH MUSCLE CELL;

EID: 84992417017     PISSN: 1073449X     EISSN: 15354970     Source Type: Journal    
DOI: 10.1164/rccm.201510-2003OC     Document Type: Article

References (50)

1. Humbert M, Morrell NW, Archer SL, Stenmark KR, MacLean MR, Lang IM, Christman BW, Weir EK, Eickelberg O, Voelkel NF, et al. Cellular and molecular pathobiology of pulmonary arterial hypertension. J Am Coll Cardiol 2004;43(Suppl. S):13S-24S.
2. Morrell NW, Adnot S, Archer SL, Dupuis J, Jones PL, MacLean MR, McMurtry IF, Stenmark KR, Thistlethwaite PA, Weissmann N, et al. Cellular and molecular basis of pulmonary arterial hypertension. J Am Coll Cardiol 2009;54(Suppl. 1)S20-S31.
3. Erzurum S, Rounds SI, Stevens T, Aldred M, Aliotta J, Archer SL, Asosingh K, Balaban R, Bauer N, Bhattacharya J, et al. Strategic plan for lung vascular research: an NHLBI-ORDR Workshop Report. Am J Respir Crit Care Med 2010;182:1554-1562.
4. de Jesus Perez V, Yuan K, Alastalo T-P, Spiekerkoetter E, Rabinovitch M. Targeting the Wnt signaling pathways in pulmonary arterial hypertension. Drug Discov Today 2014;19:1270-1276.
5. Goncharov DA, Kudryashova TV, Ziai H, Ihida-Stansbury K, DeLisser H, Krymskaya VP, Tuder RM, Kawut SM, Goncharova EA. Mammalian target of rapamycin complex 2 (mTORC2) coordinates pulmonary artery smooth muscle cell metabolism, proliferation, and survival in pulmonary arterial hypertension. Circulation 2014;129:864-874.
6. Rabinovitch M. Molecular pathogenesis of pulmonary arterial hypertension. J Clin Invest 2012;122:4306-4313.
7. West JD, Austin ED, Gaskill C, Marriott S, Baskir R, Bilousova G, Jean J-C, Hemnes AR, Menon S, Bloodworth NC, et al. Identification of a common Wnt-associated genetic signature across multiple cell types in pulmonary arterial hypertension. Am J Physiol Cell Physiol 2014; 307:C415-C430.
8. Johnson R, Halder G. The two faces of Hippo: targeting the HIPPO pathway for regenerative medicine and cancer treatment. Nat Rev Drug Discov 2014;13:63-79.
9. Chan EHY, Nousiainen M, Chalamalasetty RB, Schafer A, Nigg EA, Sillje HHW. The Ste20-like kinase Mst2 activates the human large tumor suppressor kinase Lats1. Oncogene 2005;24:2076-2086.
10. Bertero T, Cottrill KA, Lu Y, Haeger CM, Dieffenbach P, Annis S, Hale A, Bhat B, Kaimal V, Zhang YY, et al. Matrix remodeling promotes pulmonary hypertension through feedback mechanoactivation of the YAP/TAZ-miR-130/301 circuit. Cell Reports 2015;13: 1016-1032.
11. Guignabert C, Tu L, Le Hiress M, Ricard N, Sattler C, Seferian A, Huertas A, Humbert M, Montani D. Pathogenesis of pulmonary arterial hypertension: lessons from cancer. Eur Respir Rev 2013;22:543-551.
12. Schermuly RT, Ghofrani HA, Wilkins MR, Grimminger F. Mechanisms of disease: pulmonary arterial hypertension. Nat Rev Cardiol 2011;8: 443-455.
13. Rappaport N, Nativ N, Stelzer G, Twik M, Guan-Golan Y, Iny Stein T, Bahir I, Belinky F, Morrey CP, Safran M, et al. MalaCards: an integrated compendium for diseases and their annotation. Database 2013;2013:1-14.
14. Krymskaya VP, Snow J, Cesarone G, Khavin I, Goncharov DA, Lim PN, Veasey SC, Ihida-Stansbury K, Jones PL, Goncharova EA. mTOR is required for pulmonary arterial vascular smooth muscle cell proliferation under chronic hypoxia. FASEB J 2011;25:1922-1933.
15. Goncharova EA, Goncharov DA, Krymskaya VP. Assays for in vitro monitoring of human airway smooth muscle (ASM) and human pulmonary arterial vascular smooth muscle (VSM) cell migration. Nat Protoc 2006;1:2933-2939.
16. Dupont S, Morsut L, Aragona M, Enzo E, Giulitti S, Cordenonsi M, Zanconato F, Le Digabel J, Forcato M, Bicciato S, et al. Role of YAP/TAZ in mechanotransduction. Nature 2011;474:179-183.
17. Meloche J, Pflieger A, Vaillancourt M, Paulin R, Potus F, Zervopoulos S, Graydon C, Courboulin A, Breuils-Bonnet S, Tremblay E, et al. Role for DNA damage signaling in pulmonary arterial hypertension. Circulation 2014;129:786-797.
18. Taraseviciene-Stewart L, Kasahara Y, Alger L, Hirth P, Mc Mahon G, Waltenberger J, Voelkel NF, Tuder RM. Inhibition of the VEGF receptor 2 combined with chronic hypoxia causes cell deathdependent pulmonary endothelial cell proliferation and severe pulmonary hypertension. FASEB J 2001;15:427-438.
19. Kelley EE, Baust J, Bonacci G, Golin-Bisello F, Devlin JE, St Croix CM, Watkins SC, Gor S, Cantu-Medellin N, Weidert ER, et al. Fatty acid nitroalkenes ameliorate glucose intolerance and pulmonary hypertension in high-fat diet-induced obesity. Cardiovasc Res 2014;101:352-363.
20. Vitali SH, Hansmann G, Rose C, Fernandez-Gonzalez A, Scheid A,Mitsialis SA, Kourembanas S. The Sugen 5416/hypoxia mouse model of pulmonary hypertension revisited: long-term follow-up. Pulm Circ 2014;4:619-629.
21. Gomez M, Gomez V, Hergovich A. The HIPPO pathway in disease and therapy: cancer and beyond. Clin Transl Med 2014;3:22.
22. Liu-Chittenden Y, Huang B, Shim JS, Chen Q, Lee S-J, Anders RA, Liu JO, Pan D. Genetic and pharmacological disruption of the TEADYAP complex suppresses the oncogenic activity of YAP. Genes Dev 2012;26:1300-1305.
23. Igarashi Y, Eroshkin A, Gramatikova S, Gramatikoff K, Zhang Y, Smith JW, Osterman AL, Godzik A. CutDB: A proteolytic event database. Nucleic Acids Res 2007;35:D546-D549.
24. Dinkel H, Chica C, Via A, Gould CM, Jensen LJ, Gibson TJ, Diella F. Phospho.ELM: A database of phosphorylation sites-update 2011. Nucleic Acids Res 2011;39:D261-D267.
25. Orchard S, Ammari M, Aranda B, Breuza L, Briganti L, Broackes-Carter F, Campbell NH, Chavali G, Chen C, del-Toro N, et al. The MIntAct project-IntAct as a common curation platform for 11 molecular interaction databases. Nucleic Acids Res 2014;42:D358-D363.
26. Rual J-F, Venkatesan K, Hao T, Hirozane-Kishikawa T, Dricot A, Li N, Berriz GF, Gibbons FD, Dreze M, Ayivi-Guedehoussou N, et al. Towards a proteome-scale map of the human protein-protein interaction network. Nature 2005;437:1173-1178.
27. Bertero T, Lu Y, Annis S, Hale A, Bhat B, Saggar R, Saggar R, Wallace WD, Ross DJ, Vargas SO, et al. Systems-level regulation of microRNA networks by miR-130/301 promotes pulmonary hypertension. J Clin Invest 2014;124:3514-3528.
28. Tang H, Chen J, Fraidenburg DR, Song S, Sysol JR, Drennan AR, Offermanns S, Ye RD, BoniniMG,Minshall RD, et al. Deficiency of Akt1, but not Akt2, attenuates the development of pulmonary hypertension. Am J Physiol Lung Cell Mol Physiol 2015;308:L208-L220.
29. Li X, Zhang X, Leathers R, Makino A, Huang C, Parsa P, Macias J, Yuan JXJ, Jamieson SW, Thistlethwaite PA. Notch3 signaling promotes the development of pulmonary arterial hypertension. Nat Med 2009; 15:1289-1297.
30. Goncharova EA, Goncharov DA, Li H, Pimtong W, Lu S, Khavin I, Krymskaya VP. mTORC2 is required for proliferation and survival of TSC2-null cells. Mol Cell Biol 2011;31:2484-2498.
31. Guertin DA, Stevens DM, Thoreen CC, Burds AA, Kalaany NY, Moffat J, Brown M, Fitzgerald KJ, Sabatini DM. Ablation in mice of the mTORC components raptor, rictor, or mLST8 reveals that mTORC2 is required for signaling to Akt-FOXO and PKCa, but not S6K1. Dev Cell 2006;11:859-871.
32. Sarbassov DD, Guertin DA, Ali SM, Sabatini DM. Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science 2005; 307:1098-1101.
33. GagnéD, Groulx J-F, Benoit YD, Basora N, Herring E, Vachon PH, Beaulieu J-F. Integrin-linked kinase regulates migration and proliferation of human intestinal cells under a fibronectin-dependent mechanism. J Cell Physiol 2010;222:387-400.
34. Jones PL, Cowan KN, Rabinovitch M. Tenascin-C, proliferation and subendothelial fibronectin in progressive pulmonary vascular disease. Am J Pathol 1997;150:1349-1360.
35. Mitani Y, Ueda M, Komatsu R, Maruyama K, Nagai R, Matsumura M, Sakurai M. Vascular smooth muscle cell phenotypes in primary pulmonary hypertension. Eur Respir J 2001;17:316-320.
36. Wu C, Dedhar S. Integrin-linked kinase (ILK) and its interactors: A new paradigm for the coupling of extracellular matrix to actin cytoskeleton and signaling complexes. J Cell Biol 2001;155:505-510.
37. McDonald PC, Fielding AB, Dedhar S. Integrin-linked kinase: essential roles in physiology and cancer biology. J Cell Sci 2008;121:3121-3132.
38. Lee S-L, Hsu E-C, Chou C-C, Chuang H-C, Bai L-Y, Kulp SK, Chen CS. Identification and characterization of a novel integrin-linked kinase inhibitor. J Med Chem 2011;54:6364-6374.
39. Morgan JT, Murphy CJ, Russell P. What do mechanotransduction, Hippo, Wnt, and TGFb have in common? YAP and TAZ as key orchestrating molecules in ocular health and disease. Exp Eye Res 2013;115:1-12.
40. Serrano I, McDonald PC, Lock F, Muller WJ, Dedhar S. Inactivation of the Hippo tumour suppressor pathway by integrin-linked kinase. Nat Commun 2013;4:2976.
41. Shkumatov A, Thompson M, Choi KM, Sicard D, Baek K, Kim DH, Tschumperlin DJ, Prakash YS, Kong H. Matrix stiffness-modulated proliferation and secretory function of the airway smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 2015;308: L1125-L1135.
42. Ciuclan L, Bonneau O, Hussey M, Duggan N, Holmes AM, Good R, Stringer R, Jones P, Morrell NW, Jarai G, et al. A novel murine model of severe pulmonary arterial hypertension. Am J Respir Crit Care Med 2011;184:1171-1182.
43. Harvey KF, Zhang X, Thomas DM. The HIPPO pathway and human cancer. Nat Rev Cancer 2013;13:246-257.
44. Varelas X, Samavarchi-Tehrani P, Narimatsu M, Weiss A, Cockburn K, Larsen BG, Rossant J, Wrana JL. The Crumbs complex couples cell density sensing to HIPPO-dependent control of the TGF-b-SMAD pathway. Dev Cell 2010;19:831-844.
45. Varelas X, Sakuma R, Samavarchi-Tehrani P, Peerani R, Rao BM, Dembowy J, Yaffe MB, Zandstra PW, Wrana JL. TAZ controls Smad nucleocytoplasmic shuttling and regulates human embryonic stemcell self-renewal. Nat Cell Biol 2008;10:837-848.
46. Nishio M, Otsubo K, Maehama T, Mimori K, Suzuki A. Capturing the mammalian HIPPO: elucidating its role in cancer. Cancer Sci 2013; 104:1271-1277.
47. Liu J, Costello PC, Pham NA, Pintillie M, Jabali M, Sanghera J, Tsao MS, Johnston MR. Integrin-linked kinase inhibitor KP-392 demonstrates clinical benefits in an orthotopic human non-small cell lung cancer model. J Thorac Oncol 2006;1:771-779.
48. Edwards LA, Thiessen B, Dragowska WH, Daynard T, Bally MB, Dedhar S. Inhibition of ILK in PTEN-mutant human glioblastomas inhibits PKB/Akt activation, induces apoptosis, and delays tumor growth. Oncogene 2005;24:3596-3605.
49. Mikalsen T, Gertis N, Moens U. Inhibitors of signal transduction protein kinases as targets for cancer therapy. In: Raafat El-Gewely M, editor. Biotechnology annual review. Amsterdam, the Netherlands: Elsevier Science; 2006. pp. 153-224.
50. Akhmedov NB, Yamashita CK, Tran D, Piri NI, Aguirre GD, Farber DB. Two forms of the large tumor suppressor gene (Lats1) protein expressed in the vertebrate retina. Biochim Biophys Acta Gene Struct Expression 2005;1728:11-17.