AMPK and endothelial nitric oxide synthase signaling regulates KRas plasma membrane interactions via cyclic GMP-dependent protein kinase 2

Molecular and Cellular Biology

Volumn 36, Issue 24, 2016, Pages 3086-3099

  Cho, Kwang jin ^a   Casteel, Darren E ^b   Prakash, Priyanka ^a   Tan, Lingxiao ^a   van der Hoeven, Dharini ^c   Salim, Angela A ^d   Kim, Choel ^e   Capon, Robert J ^d   Lacey, Ernest ^f   Cunha, Shane R ^a   Gorfe, Alemayehu A ^a   Hancock, John F ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c UNIVERSITY OF TEXAS   (United States)

^d UNIVERSITY OF QUEENSLAND   (Australia)

^e BAYLOR COLLEGE OF MEDICINE   (United States)

^f MICROBIAL SCREENING TECHNOLOGIES PTY LTD   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC GMP DEPENDENT PROTEIN KINASE 2; ENDOTHELIAL NITRIC OXIDE SYNTHASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; K RAS PROTEIN; NITRIC OXIDE; RAS PROTEIN; SERINE; SILDENAFIL;

ANIMAL CELL; ARTICLE; BHK CELL LINE; CELL MEMBRANE; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME ACTIVATION; MDCK CELL LINE; NON SMALL CELL LUNG CANCER; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; ANIMAL; CELL LINE; CHEMISTRY; DOG; DRUG EFFECTS; ENDOCYTOSIS; GENE EXPRESSION REGULATION; HUMAN; LUNG TUMOR; METABOLISM; PHOSPHORYLATION; TUMOR CELL LINE;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; CARCINOMA, NON-SMALL-CELL LUNG; CELL LINE; CELL LINE, TUMOR; CELL MEMBRANE; CELL PROLIFERATION; CYCLIC GMP-DEPENDENT PROTEIN KINASE TYPE II; DOGS; ENDOCYTOSIS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; LUNG NEOPLASMS; MADIN DARBY CANINE KIDNEY CELLS; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE III; PHOSPHORYLATION; RAS PROTEINS; SERINE; SIGNAL TRANSDUCTION; SILDENAFIL CITRATE;

EID: 85000978479     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00365-16     Document Type: Article

References (67)

1. Hancock JF. 2003. Ras proteins: different signals from different locations. Nat Rev Mol Cell Biol 4:373-384. http://dx.doi.org/10.1038/nrm1105.
2. Hancock JF, Paterson H, Marshall CJ. 1990. A polybasic domain or palmitoylation is required in addition to the CAAX motif to localize p21ras to the plasma membrane. Cell 63:133-139. http://dx.doi.org/10.1016/0092-8674(90)90294-O.
3. Hancock JF, Magee AI, Childs JE, Marshall CJ. 1989. All Ras proteins are polyisoprenylated but only some are palmitoylated. Cell 57:1167-1177. http://dx.doi.org/10.1016/0092-8674(89)90054-8.
4. Yeung T, Gilbert GE, Shi J, Silvius J, Kapus A, Grinstein S. 2008. Membrane phosphatidylserine regulates surface charge and protein localization. Science 319:210-213. http://dx.doi.org/10.1126/science.1152066.
5. Okeley NM, Gelb MH. 2004. A designed probe for acidic phospholipids reveals the unique enriched anionic character of the cytosolic face of the mammalian plasma membrane. J Biol Chem 279:21833-21840. http://dx.doi.org/10.1074/jbc.M313469200.
6. Roy MO, Leventis R, Silvius JR. 2000. Mutational and biochemical analysis of plasma membrane targeting mediated by the farnesylated, polybasic carboxy terminus of K-ras4B. Biochemistry 39:8298-8307. http: //dx.doi.org/10.1021/bi000512q.
7. Plowman SJ, Ariotti N, Goodall A, Parton RG, Hancock JF. 2008. Electrostatic interactions positively regulate K-Ras nanocluster formation and function. Mol Cell Biol 28:4377-4385. http://dx.doi.org/10.1128 /MCB.00050-08.
8. Gutierrez L, Magee AI, Marshall CJ, Hancock JF. 1989. Posttranslational processing of p21ras is two-step and involves carboxylmethylation and carboxy-terminal proteolysis. EMBO J 8:1093-1098.
9. Hancock JF, Cadwallader K, Paterson H, Marshall CJ. 1991. A CAAX or a CAAL motif and a second signal are sufficient for plasma membrane targeting of Ras proteins. EMBO J 10:4033-4039.
10. Chandra A, Grecco HE, Pisupati V, Perera D, Cassidy L, Skoulidis F, Ismail SA, Hedberg C, Hanzal-Bayer M, Venkitaraman AR, Wittinghofer A, Bastiaens PI. 2012. The GDI-like solubilizing factor PDEdelta sustains the spatial organization and signalling of Ras family proteins. Nat Cell Biol 14:148-158. http://dx.doi.org/10.1038/ncb2394.
11. Schmick M, Vartak N, Papke B, Kovacevic M, Truxius DC, Rossmannek L, Bastiaens PI. 2014. KRas localizes to the plasma membrane by spatial cycles of solubilization, trapping and vesicular transport. Cell 157: 459-471. http://dx.doi.org/10.1016/j.cell.2014.02.051.
12. Tian T, Harding A, Inder K, Plowman S, Parton RG, Hancock JF. 2007. Plasma membrane nanoswitches generate high-fidelity Ras signal transduction. Nat Cell Biol 9:905-914. http://dx.doi.org/10.1038/ncb1615.
13. Kholodenko BN, Hancock JF, Kolch W. 2010. Signalling ballet in space and time. Nat Rev Mol Cell Biol 11:414-426. http://dx.doi.org/10.1038 /nrm2901.
14. Plowman SJ, Muncke C, Parton RG, Hancock JF. 2005. H-Ras, K-Ras, and inner plasma membrane raft proteins operate in nanoclusters with differential dependence on the actin cytoskeleton. Proc Natl Acad Sci U S A 102:15500-15505. http://dx.doi.org/10.1073/pnas.0504114102.
15. Kohnke M, Schmitt S, Ariotti N, Piggott AM, Parton RG, Lacey E, Capon RJ, Alexandrov K, Abankwa D. 2012. Design and application of in vivo FRET biosensors to identify protein prenylation and Nanoclustering inhibitors. Chem Biol 19:866-874. http://dx.doi.org/10.1016/j.chembiol.2012.05.019.
16. Zhou Y, Cho KJ, Plowman SJ, Hancock JF. 2012. Nonsteroidal antiinflammatory drugs alter the spatiotemporal organization of Ras proteins on the plasma membrane. J Biol Chem 287:16586-16595. http://dx.doi.org/10.1074/jbc.M112.348490.
17. van der Hoeven D, Cho KJ, Ma X, Chigurupati S, Parton RG, Hancock JF. 2013. Fendiline inhibits K-Ras plasma membrane localization and blocks K-Ras signal transmission. Mol Cell Biol 33:237-251. http://dx.doi.org/10.1128/MCB.00884-12.
18. Cho KJ, Park JH, Piggott AM, Salim AA, Gorfe AA, Parton RG, Capon RJ, Lacey E, Hancock JF. 2012. Staurosporines disrupt phosphatidylserine trafficking and mislocalize Ras proteins. J Biol Chem 287:43573-43584 http://dx.doi.org/10.1074/jbc.M112.424457.
19. Cho KJ, Park JH, Hancock JF. 2013. Staurosporine: a new tool for studying phosphatidylserine trafficking. Commun Integr Biol 6:e24746. http://dx.doi.org/10.4161/cib.24746.
20. Salim AA, Xiao X, Cho KJ, Piggott AM, Lacey E, Hancock JF, Capon RJ. 2014. Rare Streptomyces sp. polyketides as modulators of K-Ras localisation. Org Biomol Chem 12:4872-4878. http://dx.doi.org/10.1039/c4ob00745j.
21. Cho KJ, van der Hoeven D, Zhou Y, Maekawa M, Ma X, Chen W, Fairn GD, Hancock JF. 2015. Inhibition of acid sphingomyelinase depletes cellular phosphatidylserine and mislocalizes K-Ras from the plasma membrane. Mol Cell Biol 36:363-374. http://dx.doi.org/10.1128/MCB.00719-15.
22. Salim AA, Tan L, Huang XC, Cho KJ, Lacey E, Hancock JF, Capon RJ. 2016 Oligomycins as inhibitors of K-Ras plasma membrane localisation. Org Biomol Chem 14:711-715. http://dx.doi.org/10.1039/C5OB02020D.
23. Salim AA, Cho KJ, Tan L, Quezada M, Lacey E, Hancock JF, Capon RJ. 2014. Rare Streptomyces N-formyl amino-salicylamides inhibit oncogenic K-Ras. Org Lett 16:5036-5039. http://dx.doi.org/10.1021 /ol502376e.
24. Iglesias DA, Yates MS, van der Hoeven D, Rodkey TL, Zhang Q, Co NN, Burzawa J, Chigurupati S, Celestino J, Bowser J, Broaddus R, Hancock JF, Schmandt R, Lu KH. 2013. Another surprise from metformin: novel mechanism of action via K-Ras influences endometrial cancer response to therapy. Mol Cancer Ther 12:2847-2856. http://dx.doi.org /10.1158/1535-7163.MCT-13-0439.
25. Sasaki A, Arawaka S, Sato H, Kato T. 2015. Sensitive Western blotting for detection of endogenous Ser129-phosphorylated alpha-synuclein in intracellular and extracellular spaces. Sci Rep 5:14211. http://dx.doi.org/10.1038/srep14211.
26. Hancock JF, Prior IA. 2005. Electron microscopic imaging of Ras signaling domains. Methods 37:165-172. http://dx.doi.org/10.1016/j.ymeth.2005.05.018.
27. Prior IA, Muncke C, Parton RG, Hancock JF. 2003. Direct visualization of Ras proteins in spatially distinct cell surface microdomains. J Cell Biol 160:165-170. http://dx.doi.org/10.1083/jcb.200209091.
28. Ripley BD. 1977. Modelling spatial patterns. J R Stat Soc Series B Stat Methodol 39:172-192.
29. Diggle PJ, Mateu J, Clough HE. 2000. A comparison between parametric and non-parametric approaches to the analysis of replicated spatial point patterns. Adv Appl Probab 32:331-343.
30. Rangaswami H, Marathe N, Zhuang S, Chen Y, Yeh JC, Frangos JA, Boss GR, Pilz RB. 2009. Type II cGMP-dependent protein kinase mediates osteoblast mechanotransduction. J Biol Chem 284:14796-14808. http://dx.doi.org/10.1074/jbc.M806486200.
31. Prakash P, Zhou Y, Liang H, Hancock JF, Gorfe AA. 2016. Oncogenic K-Ras binds to an anionic membrane in two distinct orientations: a molecular dynamics analysis. Biophys J 110:1125-1138. http://dx.doi.org/10.1016/j.bpj.2016.01.019.
32. MacKerell AD, Bashford D, Bellott M, Dunbrack RL, Evanseck JD, Field MJ, Fischer S, Gao J, Guo H, Ha S, Joseph-McCarthy D, Kuchnir L, Kuczera K, Lau FT, Mattos C, Michnick S, Ngo T, Nguyen DT, Prodhom B, Reiher WE, Roux B, Schlenkrich M, Smith JC, Stote R, Straub J, Watanabe M, Wiorkiewicz-Kuczera J, Yin D, Karplus M. 1998. All-atom empirical potential for molecular modeling and dynamics studies of proteins. J Phys Chem B 102:3586-3616. http://dx.doi.org/10.1021 /jp973084f.
33. Klauda JB, Venable RM, Freites JA, O'Connor JW, Tobias DJ, Mondragon-Ramirez C, Vorobyov I, MacKerell AD, Jr, Pastor RW. 2010. Update of theCHARMMall-atom additive force field for lipids: validation on six lipid types. J Phys Chem B 114:7830-7843. http://dx.doi.org/10.1021/jp101759q.
34. Phillips JC, Braun R, Wang W, Gumbart J, Tajkhorshid E, Villa E, Chipot C, Skeel RD, Kale L, Schulten K. 2005. Scalable molecular dynamics with NAMD. J Comput Chem 26:1781-1802. http://dx.doi.org /10.1002/jcc.20289.
35. Toogood PL. 2008. Mitochondrial drugs. Curr Opin Chem Biol 12:457-463 http://dx.doi.org/10.1016/j.cbpa.2008.06.002.
36. Hardie DG. 2007. AMP-activated/SNF1 protein kinases: conserved guardians of cellular energy. Nat Rev Mol Cell Biol 8:774-785. http://dx.doi.org/10.1038/nrm2249.
37. Hardie DG. 2006. Neither LKB1 nor AMPK are the direct targets of metformin. Gastroenterology 131:973. http://dx.doi.org/10.1053/j.gastro.2006.07.032.
38. Fairn GD, Schieber NL, Ariotti N, Murphy S, Kuerschner L, Webb RI, Grinstein S, Parton RG. 2011. High-resolution mapping reveals topologically distinct cellular pools of phosphatidylserine. J Cell Biol 194:257-275. http://dx.doi.org/10.1083/jcb.201012028.
39. Bivona TG, Quatela SE, Bodemann BO, Ahearn IM, Soskis MJ, Mor A, Miura J, Wiener HH, Wright L, Saba SG, Yim D, Fein A, Perez de Castro I, Li C, Thompson CB, Cox AD, Philips MR. 2006. PKC regulates a farnesyl-electrostatic switch on K-Ras that promotes its association with Bcl-XL on mitochondria and induces apoptosis. Mol Cell 21:481-493. http://dx.doi.org/10.1016/j.molcel.2006.01.012.
40. Tegge W, Frank R, Hofmann F, Dostmann WR. 1995. Determination of cyclic nucleotide-dependent protein kinase substrate specificity by the use of peptide libraries on cellulose paper. Biochemistry 34:10569-10577.
41. Rolli-Derkinderen M, Sauzeau V, Boyer L, Lemichez E, Baron C, Henrion D, Loirand G, Pacaud P. 2005. Phosphorylation of serine 188 protects RhoA from ubiquitin/proteasome-mediated degradation in vascular smooth muscle cells. Circ Res 96:1152-1160. http://dx.doi.org/10.1161/01.RES.0000170084.88780.ea.
42. Barcelo C, Paco N, Beckett AJ, Alvarez-Moya B, Garrido E, Gelabert M, Tebar F, Jaumot M, Prior I, Agell N. 2013. Oncogenic K-ras segregates at spatially distinct plasma membrane signaling platforms according to its phosphorylation status. J Cell Sci 126:4553-4559. http://dx.doi.org/10.1242/jcs.123737.
43. Janosi L, Gorfe AA. 2010. Segregation of negatively charged phospholipids by the polycationic and farnesylated membrane anchor of Kras. Biophys J 99:3666-3674. http://dx.doi.org/10.1016/j.bpj.2010.10.031.
44. Gorfe AA, Babakhani A, McCammon JA. 2007. H-Ras protein in a bilayer: interaction and structure perturbation. J Am Chem Soc 129: 12280-12286. http://dx.doi.org/10.1021/ja073949v.
45. Gorfe AA, Hanzal-Bayer M, Abankwa D, Hancock JF, McCammon JA. 2007 Structure and dynamics of the full-length lipid-modified H-Ras protein in a 1,2-dimyristoylglycero-3-phosphocholine bilayer. J Med Chem 50:674-684. http://dx.doi.org/10.1021/jm061053f.
46. Gorfe AA, McCammon JA. 2008. Similar membrane affinity of monoand di-S-acylated Ras membrane anchors: a new twist in the role of protein lipidation. J Am Chem Soc 130:12624-12625. http://dx.doi.org/10.1021/ja805110q.
47. Reinhard M, Halbrugge M, Scheer U, Wiegand C, Jockusch BM, Walter U. 1992. The 46/50 kDa phosphoprotein VASP purified from human platelets is a novel protein associated with actin filaments and focal contacts. EMBO J 11:2063-2070.
48. Deguchi A, Soh JW, Li H, Pamukcu R, Thompson WJ, Weinstein IB. 2002 Vasodilator-stimulated phosphoprotein (VASP) phosphorylation provides a biomarker for the action of exisulind and related agents that activate protein kinase G. Mol Cancer Ther 1:803-809.
49. Smolenski A, Bachmann C, Reinhard K, Honig-Liedl P, Jarchau T, Hoschuetzky H, Walter U. 1998. Analysis and regulation of vasodilatorstimulated phosphoprotein serine 239 phosphorylation in vitro and in intact cells using a phosphospecific monoclonal antibody. J Biol Chem 273:20029-20035. http://dx.doi.org/10.1074/jbc.273.32.20029.
50. Butt E, Abel K, Krieger M, Palm D, Hoppe V, Hoppe J, Walter U. 1994. cAMP-and cGMP-dependent protein kinase phosphorylation sites of the focal adhesion vasodilator-stimulated phosphoprotein (VASP) in vitro and in intact human platelets. J Biol Chem 269:14509-14517.
51. Reger AS, Yang MP, Koide-Yoshida S, Guo E, Mehta S, Yuasa K, Liu A, Casteel DE, Kim C. 2014. Crystal structure of the cGMP-dependent protein kinase II leucine zipper and Rab11b protein complex reveals molecular details of G-kinase-specific interactions. J Biol Chem 289:25393-25403 http://dx.doi.org/10.1074/jbc.M114.575894.
52. Yeung T, Heit B, Dubuisson JF, Fairn GD, Chiu B, Inman R, Kapus A, Swanson M, Grinstein S. 2009. Contribution of phosphatidylserine to membrane surface charge and protein targeting during phagosome maturation. J Cell Biol 185:917-928. http://dx.doi.org/10.1083/jcb.200903020.
53. Grant BD, Donaldson JG. 2009. Pathways and mechanisms of endocytic recycling. Nat Rev Mol Cell Biol 10:597-608. http://dx.doi.org/10.1038 /nrm2755.
54. Hanzal-Bayer M, Renault L, Roversi P, Wittinghofer A, Hillig RC. 2002. The complex of Arl2-GTP and PDE delta: from structure to function. EMBO J 21:2095-2106. http://dx.doi.org/10.1093/emboj/21.9.2095.
55. Jang H, Abraham SJ, Chavan TS, Hitchinson B, Khavrutskii L, Tarasova NI, Nussinov R, Gaponenko V. 2015. Mechanisms of membrane binding of small GTPase K-Ras4B farnesylated hypervariable region. J Biol Chem 290:9465-9477. http://dx.doi.org/10.1074/jbc.M114.620724.
56. Fukumura D, Kashiwagi S, Jain RK. 2006. The role of nitric oxide in tumour progression. Nat Rev Cancer 6:521-534. http://dx.doi.org/10.1038/nrc1910.
57. Wang MT, Holderfield M, Galeas J, Delrosario R, To MD, Balmain A, McCormick F. 2015. K-Ras promotes tumorigenicity through suppression of non-canonical Wnt signaling. Cell 163:1237-1251. http://dx.doi.org/10.1016/j.cell.2015.10.041.
58. Shackelford DB, Shaw RJ. 2009. The LKB1-AMPK pathway: metabolism and growth control in tumour suppression. Nat Rev Cancer 9:563-575. http://dx.doi.org/10.1038/nrc2676.
59. Hemminki A, Markie D, Tomlinson I, Avizienyte E, Roth S, Loukola A, Bignell G, Warren W, Aminoff M, Hoglund P, Jarvinen H, Kristo P, Pelin K, Ridanpaa M, Salovaara R, Toro T, Bodmer W, Olschwang S, Olsen AS, Stratton MR, de la Chapelle A, Aaltonen LA. 1998. A serine/ threonine kinase gene defective in Peutz-Jeghers syndrome. Nature 391: 184-187. http://dx.doi.org/10.1038/34432.
60. Giardiello FM, Welsh SB, Hamilton SR, Offerhaus GJ, Gittelsohn AM, Booker SV, Krush AJ, Yardley JH, Luk GD. 1987. Increased risk of cancer in the Peutz-Jeghers syndrome.NEngl J Med 316:1511-1514. http: //dx.doi.org/10.1056/NEJM198706113162404.
61. Ding L, Getz G, Wheeler DA, Mardis ER, McLellan MD, Cibulskis K, Sougnez C, Greulich H, Muzny DM, Morgan MB, Fulton L, Fulton RS, Zhang Q, Wendl MC, Lawrence MS, Larson DE, Chen K, Dooling DJ, Sabo A, Hawes AC, Shen H, Jhangiani SN, Lewis LR, Hall O, Zhu Y, Mathew T, Ren Y, Yao J, Scherer SE, Clerc K, Metcalf GA, Ng B, Milosavljevic A, Gonzalez-Garay ML, Osborne JR, Meyer R, Shi X, Tang Y, Koboldt DC, Lin L, Abbott R, Miner TL, Pohl C, Fewell G, Haipek C, Schmidt H, Dunford-Shore BH, Kraja A, Crosby SD, Sawyer CS, et al. 2008. Somatic mutations affect key pathways in lung adenocarcinoma. Nature 455:1069-1075. http://dx.doi.org/10.1038/nature07423.
62. Matsumoto S, Iwakawa R, Takahashi K, Kohno T, Nakanishi Y, Matsuno Y, Suzuki K, Nakamoto M, Shimizu E, Minna JD, Yokota J. 2007. Prevalence and specificity of LKB1 genetic alterations in lung cancers. Oncogene 26:5911-5918. http://dx.doi.org/10.1038/sj.onc.1210418.
63. Lampson BL, Kendall SD, Ancrile BB, Morrison MM, Shealy MJ, Barrientos KS, Crowe MS, Kashatus DF, White RR, Gurley SB, Cardona DM, Counter CM. 2012. Targeting eNOS in pancreatic cancer. Cancer Res 72:4472-4482. http://dx.doi.org/10.1158/0008-5472.CAN-12-0057.
64. Komalavilas P, Shah PK, Jo H, Lincoln TM. 1999. Activation of mitogenactivated protein kinase pathways by cyclicGMPand cyclic GMP-dependent protein kinase in contractile vascular smooth muscle cells. J Biol Chem 274: 34301-34309. http://dx.doi.org/10.1074/jbc.274.48.34301.
65. Tao Y, Gu YJ, Cao ZH, Bian XJ, Lan T, Sang JR, Jiang L, Wang Y, Qian H, Chen YC. 2012. Endogenous cGMP-dependent protein kinase reverses EGF-induced MAPK/ERK signal transduction through phosphorylation of VASP at Ser239. Oncol Lett 4:1104-1108.
66. Wang R, Kwon IK, Thangaraju M, Singh N, Liu K, Jay P, Hofmann F, Ganapathy V, Browning DD. 2012. Type 2 cGMP-dependent protein kinase regulates proliferation and differentiation in the colonic mucosa. Am J Physiol Gastrointest Liver Physiol 303:G209-G219. http://dx.doi.org/10.1152/ajpgi.00500.2011.
67. Choy E, Chiu VK, Silletti J, Feoktistov M, Morimoto T, Michaelson D, Ivanov IE, Philips MR. 1999. Endomembrane trafficking of Ras: the CAAX motif targets proteins to the ER and Golgi. Cell 98:69-80. http://dx.doi.org/10.1016/S0092-8674(00)80607-8.