Pharmacologic inhibition of ROCK2 suppresses amyloid-β production in an Alzheimer's disease mouse model

Journal of Neuroscience

Volumn 33, Issue 49, 2013, Pages 19086-19098

  Herskowitz, Jeremy H ^a   Feng, Yangbo ^b   Mattheyses, Alexa L ^a   Hales, Chadwick M ^a   Higginbotham, Lenora A ^a   Duong, Duc M ^a   Montine, Thomas J ^c   Troncoso, Juan C ^d   Thambisetty, Madhav ^e   Seyfried, Nicholas T ^a   Levey, Allan I ^a   Lah, James J ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

^d JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e NATIONAL INSTITUTE ON AGING   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN; BETA SECRETASE 1; PROTEIN KINASE INHIBITOR; RHO ASSOCIATED COILED COIL CONTAINING PROTEIN KINASE 2; RHO KINASE; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; SR 3677; UNCLASSIFIED DRUG;

AGED; ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL VIABILITY; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DENSITOMETRY; EMBRYO; ENZYME ACTIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; GENE SILENCING; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOBLOTTING; IMMUNOCYTOCHEMISTRY; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; LIQUID CHROMATOGRAPHY; MALE; MINI MENTAL STATE EXAMINATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; TANDEM MASS SPECTROMETRY;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; AMYLOID BETA-PROTEIN PRECURSOR; AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; ASPARTIC ACID ENDOPEPTIDASES; BLOTTING, WESTERN; CELL LINE; CELL SURVIVAL; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; DNA; DOSE-RESPONSE RELATIONSHIP, DRUG; HEK293 CELLS; HUMANS; IMMUNOHISTOCHEMISTRY; LENTIVIRUS; MICE; MICROSCOPY, CONFOCAL; PLASMIDS; RHO-ASSOCIATED KINASES; STEREOTAXIC TECHNIQUES; TANDEM MASS SPECTROMETRY;

EID: 84889049013     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2508-13.2013     Document Type: Article

References (46)

1. Amano M, Tsumura Y, Taki K, Harada H, Mori K, Nishioka T, Kato K, Suzuki T, Nishioka Y, Iwamatsu A, Kaibuchi K (2010) A proteomic approach for comprehensively screening substrates of protein kinases such as Rhokinase. PLoS One 5:e8704. CrossRef Medline
2. Bolte S, Cordelières FP (2006) A guided tour into subcellular colocalization analysis in light microscopy. J Microsc 224:213-232. CrossRef Medline
3. Citron M, Teplow DB, Selkoe DJ (1995) Generation of amyloid beta protein from its precursor is sequence specific. Neuron 14:661-670. CrossRef Medline
4. Cole SL, Vassar R (2007) The Alzheimer's disease beta-secretase enzyme, BACE1. Mol Neurodegener 2:22. CrossRef Medline
5. De Strooper B, Vassar R, Golde T (2010) The secretases: enzymes with therapeutic potential in Alzheimer disease. Nat Rev Neurol 6:99-107. CrossRef Medline
6. Donovan LE, Higginbotham L, Dammer EB, Gearing M, Rees HD, Xia Q, Duong DM, Seyfried NT, Lah JJ, Levey AI (2012) Analysis of a membrane-enriched proteome from postmortem human brain tissue in Alzheimer's disease. Proteomics Clin Appl 6:201-211. CrossRef Medline
7. Driscoll I, Troncoso J (2011) Asymptomatic Alzheimer's disease: a prodrome or a state of resilience? Curr Alzheimer Res 8:330-335. CrossRef Medline
8. Feng Y, Yin Y, Weiser A, Griffin E, Cameron MD, Lin L, Ruiz C, Schürer SC, Inoue T, Rao PV, Schröter T, Lograsso P (2008) Discovery of substituted 4-(pyrazol-4-yl)-phenylbenzodioxane-2-carboxamides as potent and highly selective Rho kinase (ROCK-II) inhibitors. J Med Chem 51:6642-6645. CrossRef Medline
9. Fukumoto H, Cheung BS, Hyman BT, Irizarry MC (2002) Beta-secretase protein and activity are increased in the neocortex in Alzheimer disease. Arch Neurol 59:1381-1389. CrossRef Medline
10. Goate A, Chartier-Harlin MC, Mullan M, Brown J, Crawford F, Fidani L, Giuffra L, Haynes A, Irving N, James L, et al. (1991) Segregation of a missense mutation in the amyloid precursor protein gene with familial Alzheimer's disease. Nature 349:704-706. CrossRef
11. Haass C, Koo EH, Capell A, Teplow DB, Selkoe DJ (1995) Polarized sorting of beta-amyloid precursor protein and its proteolytic products in MDCK cells is regulated by two independent signals. J Cell Biol 128:537-547. CrossRef Medline
12. Hardy J (1997) The Alzheimer family of diseases: many etiologies, one pathogenesis? Proc Natl Acad Sci U S A 94:2095-2097. CrossRef Medline
13. Hartmann T, Bieger SC, Brühl B, Tienari PJ, Ida N, Allsop D, Roberts GW, Masters CL, Dotti CG, Unsicker K, Beyreuther K (1997) Distinct sites of intracellular production for Alzheimer's disease A beta40/42 amyloid peptides. Nat Med 3:1016-1020. CrossRef Medline
14. Herskowitz JH, Seyfried NT, Duong DM, Xia Q, Rees HD, Gearing M, Peng J, Lah JJ, Levey AI (2010) Phosphoproteomic analysis reveals site-specific changes in GFAP and NDRG2 phosphorylation in frontotemporal lobar degeneration. J Proteome Res 9:6368-6379. CrossRef Medline
15. Herskowitz JH, Seyfried NT, Gearing M, Kahn RA, Peng J, Levey AI, Lah JJ (2011) Rho kinase II phosphorylation of the lipoprotein receptor LR11/ SORLA alters amyloid-beta production. J Biol Chem 286:6117-6127. CrossRef Medline
16. Herskowitz JH, Offe K, Deshpande A, Kahn RA, Levey AI, Lah JJ (2012) GGA1-mediated endocytic traffic of LR11/SorLA alters APP intracellular distribution and amyloid-beta production. Mol Biol Cell 23:2645-2657. CrossRef Medline
17. Jonsson T, Atwal JK, Steinberg S, Snaedal J, Jonsson PV, Bjornsson S, Stefansson H, Sulem P, Gudbjartsson D, Maloney J, Hoyte K, Gustafson A, Liu Y, Lu Y, Bhangale T, Graham RR, Huttenlocher J, Bjornsdottir G, Andreassen OA, Jönsson EG, et al. (2012) A mutation in APP protects against Alzheimer's disease and age-related cognitive decline. Nature 488:96-99. CrossRef Medline
18. Karaman MW, Herrgard S, Treiber DK, Gallant P, Atteridge CE, Campbell BT, Chan KW, Ciceri P, Davis MI, Edeen PT, Faraoni R, Floyd M, Hunt JP, Lockhart DJ, Milanov ZV, Morrison MJ, Pallares G, Patel HK, Pritchard S, Wodicka LM, et al. (2008) A quantitative analysis of kinase inhibitor selectivity. Nat Biotechnol 26:127-132. CrossRef Medline
19. Koh YH, von Arnim CA, Hyman BT, Tanzi RE, Tesco G (2005) BACE is degraded via the lysosomal pathway. J Biol Chem 280:32499-32504. CrossRef Medline
20. Koo EH, Squazzo SL (1994) Evidence that production and release of amyloid beta-protein involves the endocytic pathway. J Biol Chem 269: 17386-17389. Medline
21. Lee DH, Shi J, Jeoung NH, Kim MS, Zabolotny JM, Lee SW, White MF, Wei L, Kim YB (2009) Targeted disruption of ROCK1 causes insulin resistance in vivo. J Biol Chem 284:11776-11780. CrossRef Medline
22. Lee MS, Kao SC, Lemere CA, Xia W, Tseng HC, Zhou Y, Neve R, Ahlijanian MK, Tsai LH (2003) APP processing is regulated by cytoplasmic phosphorylation. J Cell Biol 163:83-95. CrossRef Medline
23. Leuchtenberger S, Kummer MP, Kukar T, Czirr E, Teusch N, Sagi SA, Berdeaux R, Pietrzik CU, Ladd TB, Golde TE, Koo EH, Weggen S (2006) Inhibitors of Rho-kinase modulate amyloid-beta (Abeta) secretion but lack selectivity for Abeta42. J Neurochem 96:355-365. CrossRef Medline
24. Masters CL, Simms G, Weinman NA, Multhaup G, McDonald BL, Beyreuther K (1985) Amyloid plaque core protein in Alzheimer disease and Down syndrome. Proc Natl Acad Sci U S A 82:4245-4249. CrossRef Medline
25. Mullan M, Crawford F, Axelman K, Houlden H, Lilius L, Winblad B, Lannfelt L (1992) A pathogenic mutation for probable Alzheimer's disease in the APP gene at the N-terminus of beta-amyloid. Nat Genet 1:345-347. CrossRef Medline
26. Murrell J, Farlow M, Ghetti B, Benson MD (1991) A mutation in the amyloid precursor protein associated with hereditary Alzheimer's disease. Science 254:97-99. CrossRef Medline
27. Nakagawa O, Fujisawa K, Ishizaki T, Saito Y, Nakao K, Narumiya S (1996) ROCK-I and ROCK-II, two isoforms of Rho-associated coiled-coil forming protein serine/threonine kinase in mice. FEBS Lett 392:189-193. CrossRef Medline
28. Oakley H, Cole SL, Logan S, Maus E, Shao P, Craft J, Guillozet-Bongaarts A, Ohno M, Disterhoft J, Van Eldik L, Berry R, Vassar R (2006) Intraneuronal β-amyloid aggregates, neurodegeneration, and neuron loss in transgenic mice with five familial Alzheimer's disease mutations: potential factors in amyloid plaque formation. J Neurosci 26:10129-10140. CrossRef Medline
29. Oishi M, Nairn AC, Czernik AJ, Lim GS, Isohara T, Gandy SE, Greengard P, Suzuki T (1997) The cytoplasmic domain of Alzheimer's amyloid precursor protein is phosphorylated at Thr654, Ser655, and Thr668 in adult rat brain and cultured cells. Mol Med 3:111-123. Medline
30. Pedrini S, Carter TL, Prendergast G, Petanceska S, Ehrlich ME, Gandy S (2005) Modulation of statin-activated shedding of Alzheimer APP ectodomain by ROCK. PLoS Med 2:e18. CrossRef Medline
31. Ramelot TA, Nicholson LK (2001) Phosphorylation-induced structural changes in the amyloid precursor protein cytoplasmic tail detected by NMR. J Mol Biol 307:871-884. CrossRef Medline
32. Sannerud R, Declerck I, Peric A, Raemaekers T, Menendez G, Zhou L, Veerle B, Coen K, Munck S, De Strooper B, Schiavo G, Annaert W (2011) ADP ribosylation factor 6 (ARF6) controls amyloid precursor protein (APP) processing by mediating the endosomal sorting of BACE1. Proc Natl Acad Sci U S A 108:E559-E568. CrossRef Medline
33. Selkoe DJ, Podlisny MB, Joachim CL, Vickers EA, Lee G, Fritz LC, Oltersdorf T (1988) Beta-amyloid precursor protein of Alzheimer disease occurs as 110- to 135-kilodalton membrane-associated proteins in neural and nonneural tissues. Proc Natl Acad Sci U S A 85:7341-7345. CrossRef Medline
34. Shibuya M, Hirai S, Seto M, Satoh S, Ohtomo E (2005) Effects of fasudil in acute ischemic stroke: results of a prospective placebo-controlled doubleblind trial. J Neurol Sci 238:31-39. CrossRef Medline
35. Shock NW GR, Andres R, Arenberg D, Costa Jr, PT, Lakatta EG, Tobin JD (1984) Normal human aging: the Baltimore Longitudinal Study of Aging. Bethesda, MD: NIH 84-2450.
36. Sisodia SS (1992) Beta-amyloid precursor protein cleavage by a membranebound protease. Proc Natl Acad Sci U S A 89:6075-6079. CrossRef Medline
37. Sperling RA, Aisen PS, Beckett LA, Bennett DA, Craft S, Fagan AM, Iwatsubo T, Jack CR Jr, Kaye J, Montine TJ, Park DC, Reiman EM, Rowe CC, Siemers E, Stern Y, Yaffe K, Carrillo MC, Thies B, Morrison-Bogorad M, Wagster MV, et al. (2011) Toward defining the preclinical stages of Alzheimer's disease: recommendations from the National Institute on Aging-Alzheimer's Association workgroups on diagnostic guidelines for Alzheimer's disease. Alzheimers Dement 7:280-292. CrossRef Medline
38. Spoelgen R, von Arnim CA, Thomas AV, Peltan ID, Koker M, Deng A, Irizarry MC, Andersen OM, Willnow TE, Hyman BT (2006) Interaction of the cytosolic domains of sorLA/LR11 with the amyloid precursor protein (APP) and β-secretase β-site APP-cleaving enzyme. J Neurosci 26: 418-428. CrossRef Medline
39. Stachel SJ (2009) Progress toward the development of a viable BACE-1 inhibitor. Drug Dev Res 70:101-110. CrossRef
40. Totsukawa G, Yamakita Y, Yamashiro S, Hartshorne DJ, Sasaki Y, Matsumura F (2000) Distinct roles of ROCK (Rho-kinase) and MLCK in spatial regulation of MLC phosphorylation for assembly of stress fibers and focal adhesions in 3T3 fibroblasts. J Cell Biol 150:797-806. CrossRef Medline
41. Uehata M, Ishizaki T, Satoh H, Ono T, Kawahara T, Morishita T, Tamakawa H, Yamagami K, Inui J, Maekawa M, Narumiya S (1997) Calcium sensitization of smooth muscle mediated by a Rho-associated protein kinase in hypertension. Nature 389:990-994. CrossRef Medline
42. von Arnim CA, Tangredi MM, Peltan ID, Lee BM, Irizarry MC, Kinoshita A, Hyman BT (2004) Demonstration of BACE (beta-secretase) phosphorylation and its interaction with GGA1 in cells by fluorescencelifetime imaging microscopy. J Cell Sci 117:5437-5445. CrossRef Medline
43. Xu G, Stevens SM Jr, Moore BD, McClung S, Borchelt DR (2013) Cytosolic proteins lose solubility as amyloid deposits in a transgenic mouse model of Alzheimer-type amyloidosis. Hum Mol Genet 22:2765-2774. CrossRef Medline
44. Yang LB, Lindholm K, Yan R, Citron M, Xia W, Yang XL, Beach T, Sue L, Wong P, Price D, Li R, Shen Y (2003) Elevated beta-secretase expression and enzymatic activity detected in sporadic Alzheimer disease. Nat Med 9:3-4. CrossRef Medline
45. Zhang Y, Li X, Qi J, Wang J, Liu X, Zhang H, Lin SC, Meng A (2009) Rock2 controls TGFbeta signaling and inhibits mesoderm induction in zebrafish embryos. J Cell Sci 122:2197-2207. CrossRef Medline
46. Zhou Y, Su Y, Li B, Liu F, Ryder JW, Wu X, Gonzalez-DeWhitt PA, Gelfanova V, Hale JE, May PC, Paul SM, Ni B (2003) Nonsteroidal antiinflammatory drugs can lower amyloidogenic Abeta42 by inhibiting Rho. Science 302:1215-1217. CrossRef Medline