GRP78/BiP/HSPA5/Dna K is a universal therapeutic target for human disease

Journal of Cellular Physiology

Volumn 230, Issue 7, 2015, Pages 1661-1676

  Booth, Laurence ^a   Roberts, Jane L ^a   Cash, Devin R ^a   Tavallai, Seyedmehrad ^a   Jean, Sophonie ^a   Fidanza, Abigail ^b   Cruz Luna, Tanya ^b   Siembiba, Paul ^b   Cycon, Kelly A ^b   Cornelissen, Cynthia N ^a   Dent, Paul ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^b NONE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 AMINO N [4 [5 (2 PHENANTHRENYL) 3 TRIFLUOROMETHYL 1H PYRAZOL 1 YL]PHENYL]ACETAMIDE; 4 AMINO 7 TERT BUTYL 5 (4 METHYLPHENYL)PYRAZOLO[3,4 D]PYRIMIDINE; COXSACKIE VIRUS AND ADENOVIRUS RECEPTOR; GLUCOSE REGULATED PROTEIN 78; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 90; INITIATION FACTOR 2ALPHA; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; NPC1 RECEPTOR; NTCP1 RECEPTOR; PKR LIKE ENDOPLASMIC RETICULUM KINASE; PROTEIN DNAK; PROTEIN KINASE; RECA PROTEIN; SILDENAFIL; TADALAFIL; TIM1 RECEPTOR; UNCLASSIFIED DRUG; CARBOLINE DERIVATIVE; HEAT SHOCK PROTEIN; MOLECULAR CHAPERONE GRP78; PHOSPHODIESTERASE V INHIBITOR; PIPERAZINE DERIVATIVE; PURINE DERIVATIVE; PYRAZOLE DERIVATIVE; SULFONAMIDE;

ADENOVIRIDAE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CANCER; CHIKUNGUNYA ALPHAVIRUS; CONTROLLED STUDY; COXSACKIE VIRUS B4; CYTOMEGALOVIRUS; DRUG TARGETING; ESCHERICHIA COLI; HUMAN; HUMAN CELL; HUMAN RESPIRATORY SYNCYTIAL VIRUS; INFLUENZA VIRUS; MEASLES VIRUS; METHICILLIN-RESISTANT STAPHYLOCOCCUS EPIDERMIDIS; MOUSE; MUMPS VIRUS; NEISSERIA GONORRHOEAE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RUBELLA VIRUS; ANIMAL; BACTERIUM; CELL DEATH; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MULTIDRUG RESISTANCE; NEOPLASMS, EXPERIMENTAL; NUDE MOUSE; PHYSIOLOGY; TUMOR CELL LINE; VIRUS;

ADENOVIRIDAE; BACTERIA (MICROORGANISMS); EUKARYOTA; HEPATITIS B VIRUS; ORTHOMYXOVIRIDAE; PROKARYOTA; RICE STRIPE VIRUS;

ANIMALS; BACTERIA; CARBOLINES; CELL DEATH; CELL LINE, TUMOR; DRUG RESISTANCE, MULTIPLE, BACTERIAL; GENE EXPRESSION REGULATION; HEAT-SHOCK PROTEINS; HUMANS; MICE; MICE, NUDE; NEOPLASMS, EXPERIMENTAL; PHOSPHODIESTERASE 5 INHIBITORS; PIPERAZINES; PURINES; PYRAZOLES; SILDENAFIL CITRATE; SULFONAMIDES; TADALAFIL; VIRUSES;

EID: 84923074569     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.24919     Document Type: Article

References (94)

1. Anderson K, Stott EJ, Wertz GW. 1992. Intracellular processing of the human respiratory syncytial virus fusion glycoprotein: Amino acid substitutions affecting folding, transport and cleavage. J Gen Virol 73:1177-1188.
2. Black KL, Yin D, Ong JM, Hu J, Konda BM, Wang X, Ko MK, Bayan JA, Sacapano MR, Espinoza A, Irvin DK, Shu Y. 2008. PDE5 inhibitors enhance tumor permeability and efficacy of chemotherapy in a rat brain tumor model. Brain Res 1230:290-302.
3. Bolt G. 2001. The measles virus (MV) glycoproteins interact with cellular chaperones in the endoplasmic reticulum and MV infection upregulates chaperone expression. Arch Virol 146:2055-2068.
4. Booth L, Cazanave SC, Hamed HA, Yacoub A, Ogretmen B, Chen CS, Grant S, Dent P. 2012a. OSU-03012 suppresses GRP78/BiP expression that causes PERK-dependent increases in tumor cell killing. Cancer Biol Ther 13:224-236.
5. Booth L, Cruickshanks N, Ridder T, Chen CS, Grant S, Dent P. 2012b. OSU-03012 interacts with lapatinib to kill brain cancer cells. Cancer Biol Ther 13:1501-1511.
6. Booth L, Roberts JL, Cruickshanks N, Grant S, Poklepovic A, Dent P. 2014a. Regulation of OSU-03012 toxicity by ER stress proteins and ER stress-inducing drugs. Mol Cancer Ther 13:2384-2398.
7. Booth L, Roberts JL, Cruickshanks N, Tavallai S, Webb T, Samuel P, Conley A, Binion B, Young HF, Poklepovic A, Spiegel S, Dent P. 2014b. PDE5 inhibitors enhance Celecoxib killing in multiple tumor types. J Cell Physiol Oct 9 DOI: 10.1002/jcp.24843. [Epub ahead of print].
8. Booth L, Roberts JL, Cruickshanks N, Conley A, Durrant DE, Das A, Fisher PB, Kukreja RC, Grant S, Poklepovic A, Dent P. 2014c. Phosphodiesterase 5 inhibitors enhance chemotherapy killing in gastrointestinal/genitourinary cancer cells. Mol Pharmacol 85:408-419.
9. Booth L, Roberts JL, Conley A, Cruickshanks N, Ridder T, Grant S, Poklepovic A, Dent P. 2014d. HDAC inhibitors enhance the lethality of low dose salinomycin in parental and stem-like GBM cells. Cancer Biol Ther 15:305-316.
10. Bredèche MF, Ehrlich SD, Michel B. 2001. Viability of rep recA mutants depends on their capacity to cope with spontaneous oxidative damage and on the DnaK chaperone protein. J Bacteriol 183:2165-2171.
11. Burugu S, Daher A, Meurs EF, Gatignol A. 2014. HIV-1 translation and its regulation by cellular factors PKR and PACT. Virus Res Jul 23. pii S0168-S1702.
12. Carleton M, Brown DT. 1997. The formation of intramolecular disulfide bridges is required for induction of the Sindbis virus mutant ts23 phenotype. J Virol 71:7696-7703.
13. Chen WT, Zhu G, Pfaffenbach K, Kanel G, Stiles B, Lee AS. 2014. GRP78 as a regulator of liver steatosis and cancer progression mediated by loss of the tumor suppressor PTEN. Oncogene 33:4997-5005.
14. Chen Y, Brandizzi F. 2013. IRE1: ER stress sensor and cell fate executor. Trends Cell Biol 23:547-555.
15. Choi CY, Park KR, Lee JH, Jeon YJ, Liu KH, Oh S, Kim DE, Yea SS. 2007. Isoeugenol suppression of inducible nitric oxide synthase expression is mediated by down-regulation of NF-kappaB, ERK1/2, and p38 kinase. Eur J Pharmacol 576:151-159.
16. Chiu HC, Soni S, Kulp SK, Curry H, Wang D, Gunn JS, Schlesinger LS, Chen CS. 2009a. Eradication of intracellular Francisella tularensis in THP-1 human macrophages with a novel autophagy inducing agent. J Biomed Sci 16:110.
17. Chiu HC, Kulp SK, Soni S, Wang D, Gunn JS, Schlesinger LS, Chen CS. 2009b. Eradication of intracellular Salmonella enterica serovar Typhimurium with a small-molecule, host cell-directed agent. Antimicrob Agents Chemother 53:5236-5244.
18. Cortes GT, Winograd E, Wiser MF. 2003. Characterization of proteins localized to a subcellular compartment associated with an alternate secretory pathway of the malaria parasite. Mol Biochem Parasitol 129:127-135.
19. Cui W, Yu CH, Hu KQ. 2005. In vitro and in vivo effects and mechanisms of celecoxib-induced growth inhibition of human hepatocellular carcinoma cells. Clin Cancer Res 11:8213-8221.
20. Dabo S, Meurs EF. 2012. DsRNA-dependent protein kinase PKR and its role in stress, signaling and HCV infection. Viruses 4:2598-2635.
21. Das A, Xi L, Kukreja RC. 2008. Protein kinase G-dependent cardioprotective mechanism of phosphodiesterase-5 inhibition involves phosphorylation of ERK and GSK3beta. J Biol Chem 283:29572-29585.
22. Deguchi A, Thompson WJ, Weinstein IB. 2004. Activation of protein kinase G is sufficient to induce apoptosis and inhibit cell migration in colon cancer cells. Cancer Res 64:3966-3973.
23. Devan BD, Pistell PJ, Duffy KB, Kelley-Bell B, Spangler EL, Ingram DK. 2014. Phosphodiesterase inhibition facilitates cognitive restoration in rodent models of age-related memory decline. NeuroRehabilitation 34:101-111.
24. Dimcheff DE, Faasse MA, McAtee FJ, Portis JL. 2004. Endoplasmic reticulum (ER) stress induced by a neurovirulent mouse retrovirus is associated with prolonged BiP binding and retention of a viral protein in the ER. J Biol Chem 279:33782-33790.
25. Donnelly N, Gorman AM, Gupta S, Samali A. 2013. The eIF2α kinases: their structures and functions. Cell Mol Life Sci. 70:3493-3511.
26. Earl PL, Moss B, Doms RW. 1991. Folding, interaction with GRP78-BiP, assembly, and transport of the human immunodeficiency virus type 1 envelope protein. J Virol. 65:2047-2055.
27. Friebe A, Koesling D. 2009. The function of NO-sensitive guanylyl cyclase: what we can learn from genetic mouse models. Nitric Oxide. 21:149-156.
28. García-Barroso C, Ricobaraza A, Pascual-Lucas M, Unceta N, Rico AJ, Goicolea MA, Sallés J, Lanciego JL, Oyarzabal J, Franco R, Cuadrado-Tejedor M, García-Osta A. 2013. Tadalafil crosses the blood-brain barrier and reverses cognitive dysfunction in a mouse model of AD. Neuropharmacology. 64:114-123.
29. Giannini C, Sarkaria JN, Saito A, Uhm JH, Galanis E, Carlson BL, Schroeder MA, James CD. 2005. Patient tumor EGFR and PDGFRA gene amplifications retained in an invasive intracranial xenograft model of glioblastoma multiforme. Neuro Oncol 7:164-176.
30. Goodwin EC, Lipovsky A, Inoue T, Magaldi TG, Edwards AP, Van Goor KE, Paton AW, Paton JC, Atwood WJ, Tsai B, DiMaio D. 2011. BiP and multiple DNAJ molecular chaperones in the endoplasmic reticulum are required for efficient simian virus 40 infection. MBio 2 e00101-e00111.
31. Gorbatyuk MS, Gorbatyuk OS. 2013. The Molecular Chaperone GRP78/BiP as a Therapeutic Target for Neurodegenerative Disorders: A Mini Review. J Genet Syndr Gene Ther 4: pii 128.
32. Ha KS, Kim KM, Kwon YG, Bai SK, Nam WD, Yoo YM, Kim PK, Chung HT, Billiar TR, Kim YM. 2003. Nitric oxide prevents 6-hydroxydopamine-induced apoptosis in PC12 cells through cGMP-dependent PI3 kinase/Akt activation. FASEB J 17:1036-1047.
33. He B. 2006. Viruses, endoplasmic reticulum stress, and interferon responses. Cell Death Differ 13:393-403.
34. Hayden MA, Lange PA, Nakayama DK. 2001. Nitric oxide and cyclic guanosine monophosphate stimulate apoptosis via activation of the Fas-FasL pathway. J Surg Res 101:183-189.
35. Hogue BG, Nayak DP. 1992. Synthesis and processing of the influenza virus neuraminidase, a type II transmembrane glycoprotein. Virology 188:510-517.
36. Hollien J, Weissman JS. 2006. Decay of endoplasmic reticulum-localized mRNAs during the unfolded protein response. Science 313:104-107.
37. Hollien J, Lin JH, Li H, Stevens N, Walter P, Weissman JS. 2009. Regulated Ire1-dependent decay of messenger RNAs in mammalian cells. J Cell Biol 186:323-331.
38. Jensen AT, Curtis J, Montgomery J, Handman E, Theander TG. 2001. Molecular and immunological characterisation of the glucose regulated protein 78 of Leishmania donovani(1). Biochim Biophys Acta 1549:73-87.
39. Johnson AJ, Smith LL, Zhu J, Heerema NA, Jefferson S, Mone A, et al. 2005. A novel celecoxib derivative, OSU-03012, induces cytotoxicity in primary CLL cells and transformed B-cell lymphoma cell line via a caspase-and Bcl-2-independent mechanism. Blood 105:2504-2509.
40. Kang SG, Kim JS, Park K, Kim JS, Groves MD, Nam DH. 2006. Combination celecoxib and temozolomide in C6 rat glioma orthotopic model. Oncol Rep 15:7-13.
41. Karami-Tehrani F, Moeinifard M, Aghaei M, Atri M. 2012. Evaluation of PDE5 and PDE9 Expression in Benign and Malignant Breast Tumors. Arch Med Res 43:470-475.
42. Kashfi K, Rigas B. 2005. Is COX-2 a 'collateral' target in cancer prevention?. Biochem Soc Trans 33:724-727.
43. Kato M, Blanton R, Wang GR, Judson TJ, Abe Y, Myoishi M, Karas RH, Mendelsohn ME. 2012. Direct Binding and Regulation of RhoA by Cyclic GMP-dependent Protein Kinase Iα. J Biol Chem 287:41342-41351.
44. Kimata Y, Kohno K. 2011. Endoplasmic reticulum stress-sensing mechanisms in yeast and mammalian cells. Curr Opin Cell Biol 23:135-142.
45. Klenke FM, Gebhard MM, Ewerbeck V, Abdollahi A, Huber PE, Sckell A. 2006. The selective Cox-2 inhibitor celecoxib suppresses angiogenesis and growth of secondary bone tumors: an intravital microscopy study in mice. BMC Cancer 12:6-9.
46. Koehne CH, Dubois RN. 2004. COX-2 inhibition and colorectal cancer. Semin Oncol 31:12-21.
47. Komalavilas P, Shah PK, Jo H, Lincoln TM. 1999. Activation of mitogen-activated protein kinase pathways by cyclic GMP and cyclic GMP-dependent protein kinase in contractile vascular smooth muscle cells. J Biol Chem 274:34301-34309.
48. Kulp SK, Yang YT, Hung CC, Chen KF, Lai JP, Tseng PH, Fowble JW, Ward PJ, Chen CS. 2004. 3-Phosphoinositide-dependent protein kinase-1/Akt signaling represents a major cyclooxygenase-2-independent target for celecoxib in prostate cancer cells. Cancer Res 64:1444-1451.
49. Kwan BW, Osbourne DO, Hu Y, Benedik MJ, Wood TK. 2014. Phosphodiesterase DosP increases persistence by reducing cAMP which reduces the signal indole. Biotechnol Bioeng Sep 12 .[Epub ahead of print].
50. Lee AS. 2007. GRP78 induction in cancer: therapeutic and prognostic implications. Cancer Res 67:3496-3499.
51. Luo B, Lee AS. 2013. The critical roles of endoplasmic reticulum chaperones and unfolded protein response in tumorigenesis and anticancer therapies. Oncogene 32:805-818.
52. Maurel M, Chevet E, Tavernier J, Gerlo S. 2014. Getting RIDD of RNA: IRE1 in cell fate regulation. Trends Biochem Sci 39:245-254.
53. Mirazimi A, Svensson L. 2000. ATP is required for correct folding and disulfide bond formation of rotavirus VP7. J Virol 74:8048-8052.
54. Moreno JA, Tiffany-Castiglioni E. 2014. The Chaperone Grp78 in protein folding disorders of the nervous system. Neurochem Res Aug 9. [Epub ahead of print].
55. Narayanan BA, Narayanan NK, Pittman B, Reddy BS. 2006. Adenocarcina of the mouse prostate growth inhibition by celecoxib: Downregulation of transcription factors involved in COX-2 inhibition. Prostate 66:257-265.
56. Ni M, Lee AS. 2007. ER chaperones in mammalian development and human diseases. FEBS Lett 581:3641-3651.
57. Noguchi A, Ikeda A, Mezaki M, Fukumori Y, Kanemori M. 2014. DnaJ-promoted binding of DnaK to multiple sites on σ32 in the presence of ATP. J Bacteriol 196:1694-1703.
58. Ostberg KL, DeRocco AJ, Mistry SD, Dickinson MK, Cornelissen CN. 2013. Conserved regions of gonococcal TbpB are critical for surface exposure and transferrin iron utilization. Infect Immun 81:3442-3450.
59. Panner A, Murray JC, Berger MS, Pieper RO. 2007. Heat shock protein 90alpha recruits FLIPS to the death-inducing signaling complex and contributes to TRAIL resistance in human glioma. Cancer Res 67:9482-9489.
60. Park MA, Yacoub A, Rahmani M, Zhang G, Hart L, Hagan MP, et al. 2008. OSU-03012 stimulates PKR-like endoplasmic reticulum-dependent increases in 70-kDa heat shock protein expression, attenuating its lethal actions in transformed cells. Mol Pharmacol 73:1168-1184.
61. Patel MI, Subbaramaiah K, Du B, Chang M, Newman RA, Cordon-Cardo C, Thaler HT, Dannenberg AJ. 2005. Celecoxib inhibits prostate cancer growth: Evidence of a cyclooxygenase-2-independent mechanism. Clin Cancer Res 11:1999-2007.
62. Pavitt GD, Ron D. 2012. New insights into translational regulation in the endoplasmic reticulum unfolded protein response. Cold Spring Harb Perspect Biol 4: .pii: a 012278..
63. Potter LR. 2011. Guanylyl cyclase structure, function and regulation. Cell Signal 23:1921-1926.
64. Quinones QJ, de Ridder GG, Pizzo SV. 2008. GRP78: A chaperone with diverse roles beyond the endoplasmic reticulum. Histol Histopathol 23:1409-1416.
65. Rao R, Fiskus W, Ganguly S, Kambhampati S, Bhalla KN. 2012. HDAC inhibitors and chaperone function. Adv Cancer Res. 116:239-262.
66. Rathore APS, Ng ML, Vasudevan SG. 2013. Differential unfolded protein response during Chikungunya and Sindbis virus infection: CHIKV nsP4 suppresses eIF2α phosphorylation. Virology Journal 10:36.
67. Reid SP, Shurtleff AC, Costantino JA, Tritsch SR, Retterer C, Spurgers KB, Bavari S. 2014. HSPA5 is an essential host factor for Ebola virus infection. Antiviral Res 109:171-174.
68. Roberts JL, Booth L, Conley A, Cruickshanks N, Malkin M, Kukreja RC, Grant S, Poklepovic A, Dent P. 2014. PDE5 inhibitors enhance the lethality of standard of care chemotherapy in pediatric CNS tumor cells. Cancer Biol Ther 15:758-767.
69. Roller C, Maddalo D. 2013. The molecular chaperone GRP78/BiP in the development of chemoresistance: Mechanism and possible treatment. Front Pharmacol. 11; 4:10.
70. Roux L. 1990. Selective and transient association of Sendai virus HN glycoprotein with BiP. Virology 175:161-166.
71. Sano R, Reed JC. 2013. ER stress-induced cell death mechanisms. Biochim Biophys Acta 1833:3460-3470.
72. Sarfati M, Mateo V, Baudet S, Rubio M, Fernandez C, Davi F, Binet JL, Delic J, Merle-Beral H. 2003. Sildenafil and vardenafil, types 5 and 6 phosphodiesterase inhibitors, induce caspase-dependent apoptosis of B-chronic lymphocytic leukemia cells. Blood 101:265-269.
73. Schmidt AJ, Ryjenkov DA, Gomelsky M. 2005. The ubiquitous protein domain EAL is a cyclic diguanylate-specific phosphodiesterase: Enzymatically active and inactive EAL domains. J Bacteriol 187:4774-4781.
74. Shan X, Quaile MP, Monk JK, French B, Cappola TP, Margulies KB. 2012. Differential expression of PDE5 in failing and nonfailing human myocardium. Circ Heart Fail 5:79-86.
75. Shen Y, Meunier L, Hendershot LM. 2002. Identification and characterization of a novel endoplasmic reticulum (ER) DnaJ homologue, which stimulates ATPase activity of BiP in vitro and is induced by ER stress. J Biol Chem. 277:15947-15956.
76. Spurgers KB, Alefantis T, Peyser BD, Ruthel GT, Bergeron AA, Costantino JA, Enterlein S, Kota KP, Boltz RC, Aman MJ, Delvecchio VG, Bavari S. 2010. Identification of essential filovirion-associated host factors by serial proteomic analysis and RNAi screen. Mol Cell Proteomics 9:2690-2703.
77. Thompson WJ, Piazza GA, Li H, Liu L, Fetter J, Zhu B, Sperl G, Ahnen D, Pamukcu R. 2000. Exisulind induction of apoptosis involves guanosine 3', 5'-cyclic monophosphate phosphodiesterase inhibition, protein kinase G activation, and attenuated beta-catenin. Cancer Res 60:3338-3342.
78. Tong L, Heim RA, Wu S. 2011. Nitric oxide: a regulator of eukaryotic initiation factor 2 kinases. Free Radic Biol Med 50:1717-1725.
79. Tuckerman JR, Gonzalez G, Gilles-Gonzalez MA. 2011. Cyclic di-GMP activation of polynucleotide phosphorylase signal-dependent RNA processing. J Mol Biol 407:633-639.
80. Vélez Acevedo RN, Ronpirin C, Kandler JL, Shafer WM, Cornelissen CN. 2014. Identification of regulatory elements that control expression of the tbpBA operon in Neisseria gonorrhoeae. J Bacteriol 196:2762-2774.
81. Xu A, Bellamy AR, Taylor JA. 1998. BiP (GRP78) and endoplasmin (GRP94) are induced following rotavirus infection and bind transiently to an endoplasmic reticulum-localized virion component. J Virol 72:9865-9872.
82. Xu Z, Jensen G, Yen TS. 1997. Activation of hepatitis B virus S promoter by the viral large surface protein via induction of stress in the endoplasmic reticulum. J Virol 71:7387-7392.
83. Yacoub A, Park MA, Hanna D, Hong Y, Mitchell C, Pandya AP, et al. 2006. OSU-03012 promotes caspase-independent but PERK-, cathepsin B-, BID-, and AIF-dependent killing of transformed cells. Mol Pharmacol 70:589-603.
84. Yang Y, Chen S, Zhang J, Li C, Sun Y, Zhang L, Zheng X. 2014. Stimulation of autophagy prevents amyloid-β peptide-induced neuritic degeneration in PC12 cells. J Alzheimers Dis 40:929-939.
85. Yu H, Li S, Yang C, Wei M, Song C, Zheng Z, Gu Y, Du H, Zhang J, Xia N. 2011. Homology model and potential virus-capsid binding site of a putative HEV receptor Grp78. J Mol Model 17:987-995.
86. Zhang X, Yan G, Ji J, Wu J, Sun X, Shen J, Jiang H, Wang H. 2012. PDE5 inhibitor promotes melanin synthesis through the PKG pathway in B16 melanoma cells. J Cell Biochem 113:2738-2743.
87. Zhang J, Guo J, Zhao X, Chen Z, Wang G, Liu A, Wang Q, Zhou W, Xu Y, Wang C. 2013. Phosphodiesterase-5 inhibitor sildenafil prevents neuroinflammation, lowers beta-amyloid levels and improves cognitive performance in APP/PS1 transgenic mice. Behav Brain Res 250:230-237.
88. Zhang S, Sun Y, Chen H, Dai Y, Zhan Y, Yu S, Qiu X, Tan L, Song C, Ding C. 2014. Activation of the PKR/eIF2α signaling cascade inhibits replication of Newcastle disease virus. Virol J 11:62.
89. Zhu B, Vemavarapu L, Thompson WJ, Strada SJ. 2005. Suppression of cyclic GMP-specific phosphodiesterase 5 promotes apoptosis and inhibits growth in HT29 cells. J Cell Biochem 94:336-350.
90. Zhu B, Strada SJ. 2007. The novel functions of cGMP-specific phosphodiesterase 5 and its inhibitors in carcinoma cells and pulmonary/cardiovascular vessels. Curr Top Med Chem 7:437-454.
91. Zhu B, Strada S, Stevens T. 2005a. Cyclic GMP-specific phosphodiesterase 5 regulates growth and apoptosis in pulmonary endothelial cells. Am J Physiol Lung Cell Mol Physiol 289:L196-L206.
92. Zhu B, Zhang L, Alexeyev M, Alvarez DF, Strada SJ, Stevens T. 2009. Type 5 phosphodiesterase expression is a critical determinant of the endothelial cell angiogenic phenotype. Am J Physiol Lung Cell Mol Physiol 296:L220-L228.
93. Zhu J, Huang JW, Tseng PH, Yang YT, Fowble JW, Shiau CW, et al. 2004. From the cyclooxygenase-2 inhibitor celecoxib to a novel class of 3-phosphoinositide-dependent protein kinase-1 inhibitors. Cancer Res 64:4309-4318.
94. Zusman RM, Morales A, Glasser DB, Osterloh IH. 1999. Overall cardiovascular profile of sildenafil citrate. Am J Cardiol 83:35C-44C.