CHIP: A new modulator of human malignant disorders

Oncotarget

Volumn 7, Issue 20, 2016, Pages 29864-29874

  Cao, Zhe ^a   Li, Guanqiao ^a   Shao, Qianqian ^a   Yang, Gang ^a   Zheng, Lianfang ^a   Zhang, Taiping ^a   Zhao, Yupei ^a  

^a PEKING UNION MEDICAL COLLEGE HOSPITAL   (China)

Author keywords

Cancer; CHIP; Co chaperon; Ubiquitination

Indexed keywords

ANDROGEN RECEPTOR; BINDING PROTEIN; CARBOXYL TERMINUS OF HSC70 INTERACTING PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR 2; GELDANAMYCIN; GLUCOCORTICOID RECEPTOR; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 90 INHIBITOR; HYPOXIA INDUCIBLE FACTOR 1ALPHA; INITIATION FACTOR 5A; MITOGEN ACTIVATED PROTEIN KINASE; MYC PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; PROTEIN P53; SCATTER FACTOR RECEPTOR; TOLL LIKE RECEPTOR; TRANSFORMING GROWTH FACTOR BETA; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; VORINOSTAT; STUB1 PROTEIN, HUMAN; UBIQUITIN PROTEIN LIGASE;

ALZHEIMER DISEASE; APOPTOSIS; ARTICLE; BREAST CANCER; CARCINOGENESIS; CHRONIC MYELOID LEUKEMIA; COLORECTAL CANCER; ESOPHAGUS CANCER; GALLBLADDER CANCER; HEART MUSCLE ISCHEMIA; HEART PROTECTION; HUMAN; LUNG CANCER; METASTASIS; NEOPLASM; NONHUMAN; ONCOGENE; PANCREAS CANCER; PARKINSON DISEASE; PATHOGENESIS; PROSTATE CANCER; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; STOMACH CANCER; TUMOR GROWTH; METABOLISM; PATHOLOGY;

HUMANS; NEOPLASMS; UBIQUITIN-PROTEIN LIGASES;

EID: 84969764478     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.8219     Document Type: Article

References (91)

1. Schubert U, Antón LC, Gibbs J, Norbury CC, Yewdell JW, Bennink JR. Rapid degradation of a large fraction of newly synthesized proteins by proteasomes. Nature. 2000; 404: 770-774.
2. Wickner S, Maurizi MR, Gottesman S. Posttranslational quality control: folding, refolding, and degrading proteins. Science. 1999; 286: 1888-1893.
3. Broadley SA, Hartl FU. The role of molecular chaperones in human misfolding diseases. FEBS Lett. 2009; 583: 2647- 2653.
4. Ballinger CA, Connell P, Wu Y, Hu Z, Thompson LJ, Yin LY, Patterson C. Identification of CHIP, a novel tetratricopeptide repeat-containing protein that interacts with heat shock proteins and negatively regulates chaperone functions. Mol Cell Biol. 1999; 19: 4535-4545.
5. Connell P, Ballinger CA, Jiang J, Wu Y, Thompson LJ, Höhfeld J, Patterson C. The co-chaperone CHIP regulates protein triage decisions mediated by heat-shock proteins. Nat Cell Biol. 2001; 3: 93-96.
6. Jiang J, Ballinger CA, Wu Y, Dai Q, Cyr DM, Höhfeld J, Patterson C. CHIP is a U-box-dependent E3 ubiquitin ligase: identification of Hsc70 as a target for ubiquitylation. J Biol Chem. 2001; 276: 42938-42944.
7. Paul I, Ghosh MK. A CHIPotle in physiology and disease. Int J Biochem Cell Biol. 2015; 58: 37-52.
8. Zhang M, Windheim M, Roe SM, Peggie M, Cohen P, Prodromou C, Pearl LH. Chaperoned ubiquitylation-- crystal structures of the CHIP U box E3 ubiquitin ligase and a CHIP-Ubc13-Uev1a complex. Mol Cell. 2005; 20: 525-538.
9. Matsumura Y, Sakai J, Skach WR. Endoplasmic reticulum protein quality control is determined by cooperative interactions between Hsp/c70 protein and the CHIP E3 ligase. J Biol Chem. 2013; 288: 31069-31079.
10. Young JC, Moarefi I, Hartl FU. Hsp90: a specialized but essential protein-folding tool. J Cell Biol. 2001; 154: 267- 273.
11. Minami Y, Hohfeld J, Ohtsuka K, Hartl FU. Regulation of the heat-shock protein 70 reaction cycle by the mammalian DnaJ homolog, Hsp40. J Biol Chem. 1996; 271: 19617- 19624.
12. McDonough H, Patterson C. CHIP: a link between the chaperone and proteasome systems. Cell Stress Chaperones. 2003; 8: 303-308 (2003).
13. Cyr DM, Hohfeld J, Patterson C. Protein quality control: U-box-containing E3 ubiquitin ligases join the fold. Trends Biochem Sci. 2002; 27: 368-375 (2002).
14. Demand J, Alberti S, Patterson C, Hohfeld J. Cooperation of a ubiquitin domain protein and an E3 ubiquitin ligase during chaperone/proteasome coupling. Curr Biol. 2001; 11: 1569- 1577.
15. Arndt V, Daniel C, Nastainczyk W, Alberti S, Hohfeld J. BAG-2 acts as an inhibitor of the chaperone-associated ubiquitin ligase CHIP. Mol Biol Cell. 2005; 16: 5891-5900.
16. Yenari MA, Liu J, Zheng Z, Vexler ZS, Lee JE, Giffard RG. Antiapoptotic and anti-inflammatory mechanisms of heat-shock protein protection. Ann N Y Acad Sci. 2005; 1053: 74-83.
17. Yang S, Qu S, Perez-Tores M, Sawai A, Rosen N, Solit DB, Arteaga CL. Association with Hsp90 inhibits Cblmediated down-regulation of mutant epidermal growth factor receptors. Cancer Res. 2006; 66: 6990-6997.
18. Wang X, DeFranco DB. Alternative effects of the ubiquitinproteasome pathway on glucocorticoid receptor downregulation and transactivation are mediated by CHIP, an E3 ligase. Mol Endocrinol. 2005; 19: 1474-1482.
19. Shin Y, Klucken J, Patterson C, Hyman BT, McLean PJ. The co-chaperone carboxyl terminus of Hsp70-interacting protein (CHIP) mediates alpha-synuclein degradation decisions between proteasomal and lysosomal pathways. J Biol Chem. 2005; 280: 23727-23734.
20. Rees I, Lee S, Kim H, Tsai FT. The E3 ubiquitin ligase CHIP binds the androgen receptor in a phosphorylationdependent manner. Biochim Biophys Acta. 2006; 1764: 1073-1079.
21. Fan M, Park A, Nephew KP. CHIP (carboxyl terminus of Hsc70-interacting protein) promotes basal and geldanamycin-induced degradation of estrogen receptoralpha. Mol Endocrinol. 2005; 19: 2901-2914 (2005).
22. Rosser MF, Washburn E, Muchowski PJ, Patterson C, Cyr DM. Chaperone functions of the E3 ubiquitin ligase CHIP. J Biol Chem. 2007; 282: 22267-22277.
23. Murata S, Minami Y, Minami M, Chiba T, Tanaka K. CHIP is a chaperone-dependent E3 ligase that ubiquitylates unfolded protein. EMBO Rep. 2001; 2: 1133-1138 (2001).
24. Dai Q, Zhang C, Wu Y, McDonough H, Whaley RA, Godfrey V, Li HH, Madamanchi N, Xu W, Neckers L, Cyr D, Patterson C. CHIP activates HSF1 and confers protection against apoptosis and cellular stress. EMBO J. 2003; 22: 5446-5458 (2003).
25. Qian SB, McDonough H, Boellmann F, Cyr DM, Patterson C. CHIP-mediated stress recovery by sequential ubiquitination of substrates and Hsp70. Nature. 2006; 440: 551-555.
26. Tan M, Yu D. Molecular mechanisms of erbB2-mediated breast cancer chemoresistance. Adv Exp Med Biol. 2007; 608: 119-129.
27. Xu W, Marcu M, Yuan X, Mimnaugh E, Patterson C, Neckers L. Chaperone-dependent E3 ubiquitin ligase CHIP mediates a degradative pathway for c-ErbB2/Neu. Proc Natl Acad Sci U S A. 2002; 99: 12847-12852.
28. Birchmeier C, Gherardi E. Developmental roles of HGF/ SF and its receptor, the c-Met tyrosine kinase. Trends Cell Biol. 1998; 8: 404-410.
29. Jang KW, Lee JE, Kim SY, Kang MW, Na MH, Lee CS, Song KS, Lim SP. The C-terminus of Hsp70- interacting protein promotes Met receptor degradation. J Thorac Oncol. 2011; 6: 679-687.
30. Slotman JA, da Silva Almeida AC, Hassink GC, van de Ven RH, van Kerkhof P, Kuiken HJ, Strous GJ. Ubc13 and COOH terminus of Hsp70-interacting protein (CHIP) are required for growth hormone receptor endocytosis. J Biol Chem. 2012; 287: 15533-15543.
31. He B, Bai S, Hnat AT, Kalman RI, Minges JT, Patterson C, Wilson EM. An androgen receptor NH2-terminal conserved motif interacts with the COOH terminus of the Hsp70-interacting protein (CHIP). J Biol Chem. 2004; 279: 30643-30653.
32. Sarkar S, Brautigan DL, Parsons SJ, Larner JM. Androgen receptor degradation by the E3 ligase CHIP modulates mitotic arrest in prostate cancer cells. Oncogene. 2014; 33: 26-33.
33. Adachi H, Waza M, Tokui K, Katsuno M, Minamiyama M, Tanaka F, Doyu M, Sobue G. CHIP overexpression reduces mutant androgen receptor protein and ameliorates phenotypes of the spinal and bulbar muscular atrophy transgenic mouse model. J Neurosci. 2007; 27: 5115-5126.
34. Tateishi Y, Kawabe Y, Chiba T, Murata S, Ichikawa K, Murayama A, Tanaka K, Baba T, Kato S, Yanagisawa J. Ligand-dependent switching of ubiquitinproteasome pathways for estrogen receptor. EMBO J. 2004; 23: 4813-4823.
35. Yi X, Wei W, Wang SY, Du ZY, Xu YJ, Yu XD. Histone deacetylase inhibitor SAHA induces ERalpha degradation in breast cancer MCF-7 cells by CHIP-mediated ubiquitin pathway and inhibits survival signaling. Biochem Pharmacol. 2008; 75: 1697-1705.
36. Jiang BH, Liu LZ. PI3K/PTEN signaling in tumorigenesis and angiogenesis. Biochim Biophys Acta. 2008; 1784: 150- 158.
37. Su CH, Wang CY, Lan KH, Li CP, Chao Y, Lin HC, Lee SD, Lee WP. Akt phosphorylation at Thr308 and Ser473 is required for CHIP-mediated ubiquitination of the kinase. Cell Signal. 2011; 23: 1824-1830.
38. Ahmed SF, Deb S, Paul I, Chatterjee A, Mandal T, Chatterjee U, Ghosh MK. The chaperone-assisted E3 ligase C terminus of Hsc70-interacting protein (CHIP) targets PTEN for proteasomal degradation. J Biol Chem. 2012; 287: 15996-16006.
39. Wang S, Wu X, Zhang J, Chen Y, Xu J, Xia X, He S, Qiang F, Li A, Shu Y, Røe OD, Li G, Zhou JW. CHIP functions as a novel suppressor of tumour angiogenesis with prognostic significance in human gastric cancer. Gut. 2013; 62: 496-508.
40. Pearson G, Robinson F, Beers Gibson T, Xu BE, Karandikar M, Berman K, Cobb MH. Mitogenactivated protein (MAP) kinase pathways: regulation and physiological functions. Endocr Rev. 2001; 22: 153-183.
41. Assaife-Lopes N, Wengert M, de Sa Pinheiro AA, Leao- Ferreira LR, Caruso-Neves C. Inhibition of renal Na+- ATPase activity by inosine is mediated by A1 receptorinduced inhibition of the cAMP signaling pathway. Arch Biochem Biophys. 2009; 489: 76-81.
42. Gao Y, Han C, Huang H, Xin Y, Xu Y, Luo L, Yin Z. eHeat shock protein 70 together with its co-chaperone CHIP inhibits TNF-alpha induced apoptosis by promoting proteasomal degradation of apoptosis signal-regulating kinase1. Apoptosis. 2010; 15: 822-833.
43. Hwang JR, Zhang C, Patterson C. C-terminus of heat shock protein 70-interacting protein facilitates degradation of apoptosis signal-regulating kinase 1 and inhibits apoptosis signal-regulating kinase 1-dependent apoptosis. Cell Stress Chaperones. 2005; 10: 147-156.
44. Sonoyama T, Sakai A, Mita Y, Yasuda Y, Kawamoto H, Yagi T, Yoshioka M, Mimura T, Nakachi K, Ouchida M, Yamamoto K, Shimizu K. TP53 codon 72 polymorphism is associated with pancreatic cancer risk in males, smokers and drinkers. Mol Med Rep. 2011; 4: 489- 495.
45. Haines DS, Landers JE, Engle LJ, George DL. Physical and functional interaction between wild-type p53 and mdm2 proteins. Mol Cell Biol. 1994; 14: 1171-1178.
46. Esser C, Scheffner M, Hohfeld J. The chaperone-associated ubiquitin ligase CHIP is able to target p53 for proteasomal degradation. J Biol Chem. 2005; 280: 27443-27448.
47. Tripathi V, Ali A, Bhat R, Pati U. CHIP chaperones wild type p53 tumor suppressor protein. J Biol Chem. 2007; 282: 28441-28454.
48. Horikawa I, Fujita K, Jenkins LM, Hiyoshi Y, Mondal AM, Vojtesek B, Lane DP, Appella E, Harris CC. Autophagic degradation of the inhibitory p53 isoform Delta133p53alpha as a regulatory mechanism for p53- mediated senescence. Nat Commun. 2014; 5: 4706.
49. Massaous J, Hata A. TGF-beta signalling through the Smad pathway. Trends Cell Biol. 1997; 7: 187-192.
50. Perlman R, Schiemann WP, Brooks MW, Lodish HF, Weinberg RA. TGF-beta-induced apoptosis is mediated by the adapter protein Daxx that facilitates JNK activation. Nat Cell Biol. 2001; 3: 708-714.
51. Shang Y, Xu X, Duan X, Guo J, Wang Y, Ren F, He D, Chang Z. Hsp70 and Hsp90 oppositely regulate TGFbeta signaling through CHIP/Stub1. Biochem Biophys Res Commun. 2014; 446: 387-392.
52. Li Q, Wang X, Wu X, Rui Y, Liu W, Wang J, Wang X, Liou YC, Ye Z, Lin SC. Daxx cooperates with the Axin/HIPK2/p53 complex to induce cell death. Cancer Res. 2007; 67: 66-74.
53. McDonough H, Charles PC, Hilliard EG, Qian SB, Min JN, Portbury A, Cyr DM, Patterson C. eStress-dependent Daxx-CHIP interaction suppresses the p53 apoptotic program. J Biol Chem. 2009; 284: 20649-20659.
54. Yang M, Wang C, Zhu X, Tang S, Shi L, Cao X, Chen T. eE3 ubiquitin ligase CHIP facilitates Toll-like receptor signaling by recruiting and polyubiquitinating Src and atypical PKC{zeta}. J Exp Med. 2011; 208: 2099-2112.
55. Sun C, Li HL, Shi ML, Liu QH, Bai J, Zheng JN. Diverse roles of C-terminal Hsp70-interacting protein (CHIP) in tumorigenesis. J Cancer Res Clin Oncol. 2014; 140: 189- 197.
56. Kajiro M, Hirota R, Nakajima Y, Kawanowa K, So-ma K, Ito I, Yamaguchi Y, Ohie SH, Kobayashi Y, Seino Y, Kawano M, Kawabe Y, Takei H, et al. The ubiquitin ligase CHIP acts as an upstream regulator of oncogenic pathways. Nat Cell Biol. 2009; 11: 312-319.
57. Tsuchiya M, Nakajima Y, Hirata N, Morishita T, Kishimoto H, Kanda Y, Kimura K. Ubiquitin ligase CHIP suppresses cancer stem cell properties in a population of breast cancer cells. Biochem Biophys Res Commun. 2014; 452: 928-932.
58. Patani N, Jiang W, Newbold R, Mokbel K. Prognostic implications of carboxyl-terminus of Hsc70 interacting protein and lysyl-oxidase expression in human breast cancer. J Carcinog. 2010; 9: 9.
59. Wang T, Yang J, Xu J, Li J, Cao Z, Zhou L, You L, Shu H, Lu Z, Li H, Li M, Zhang T, Zhao Y. CHIP is a novel tumor suppressor in pancreatic cancer through targeting EGFR. Oncotarget. 2014; 5: 1969-1986. doi: 10.18632/ oncotarget.1890.
60. Gan L, Liu DB, Lu HF, Long GX, Mei Q, Hu GY, Qiu H, Hu GQ. Decreased expression of the carboxyl terminus of heat shock cognate 70 interacting protein in human gastric cancer and its clinical significance. Oncol Rep. 2012; 28: 1392-1398.
61. Wang Y, Ren F, Wang Y, Feng Y, Wang D, Jia B, Qiu Y, Wang S, Yu J, Sung JJ, Xu J, Zeps N, Chang Z. CHIP/Stub1 functions as a tumor suppressor and represses NF-kappaB-mediated signaling in colorectal cancer. Carcinogenesis. 2014; 35: 983-991.
62. Tsukahara F, Maru Y. Bag1 directly routes immature BCRABL for proteasomal degradation. Blood. 2010; 116: 3582- 3592.
63. Shang Y, Zhao X, Tian B, Wang Y, Ren F, Jia B, Zhai Y, Chen W, He D, Chang Z. CHIP/Stub1 interacts with eIF5A and mediates its degradation. Cell Signal. 2014; 26: 1098-1104.
64. Su CH, Lan KH, Li CP, Chao Y, Lin HC, Lee SD, Lee WP. ePhosphorylation accelerates geldanamycin-induced Akt degradation. Arch Biochem Biophys. 2013; 536: 6-11.
65. Paul I, Ahmed SF, Bhowmik A, Deb S, Ghosh MK. The ubiquitin ligase CHIP regulates c-Myc stability and transcriptional activity. Oncogene. 2013; 32: 1284-1295.
66. Bento CF, Fernandes R, Ramalho J, Marques C, Shang F, Taylor A, Pereira P. The chaperone-dependent ubiquitin ligase CHIP targets HIF-1alpha for degradation in the presence of methylglyoxal. PloS One. 2010; 5: e15062.
67. Ferreira JV, Fôfo H, Bejarano E, Bento CF, Ramalho JS, Girão H, Pereira P. STUB1/CHIP is required for HIF1A degradation by chaperone-mediated autophagy. Autophagy. 2013; 9: 1349-1366.
68. Ferreira JV, Soares AR, Ramalho JS, Pereira P, Girao H. K63 linked ubiquitin chain formation is a signal for HIF1A degradation by chaperone-mediated autophagy. Sci Rep. 2015; 5: 10210.
69. Li F, Xie P, Fan Y, Zhang H, Zheng L, Gu D, Patterson C, Li H. C terminus of Hsc70-interacting protein promotes smooth muscle cell proliferation and survival through ubiquitin-mediated degradation of FoxO1. J Biol Chem. 2009; 284: 20090-20098.
70. Oh KH, Yang SW, Park JM, Seol JH, Iemura S, Natsume T, Murata S, Tanaka K, Jeon YJ, Chung CH. Control of AIF-mediated cell death by antagonistic functions of CHIP ubiquitin E3 ligase and USP2 deubiquitinating enzyme. Cell Death Differ. 2011; 18: 1326-1336.
71. Narayan V, Pion E, Landre V, Muller P, Ball KL. Dockingdependent ubiquitination of the interferon regulatory factor-1 tumor suppressor protein by the ubiquitin ligase CHIP. J Biol Chem. 2011; 286: 607-619.
72. Liang ZL, Kim M, Huang SM, Lee HJ, Kim JM. Expression of carboxyl terminus of Hsp70-interacting protein (CHIP) indicates poor prognosis in human gallbladder carcinoma. Oncol Lett. 2013; 5: 813-818.
73. Wen J, Luo KJ, Hu Y, Yang H, Fu JH. Metastatic lymph node CHIP expression is a potential prognostic marker for resected esophageal squamous cell carcinoma patients. Ann Surg Oncol. 2013; 20: 1668-1675.
74. Moore DJ, West AB, Dawson VL, Dawson TM. Molecular pathophysiology of Parkinson's disease. Annu Rev Neurosci. 2005; 28: 57-87.
75. Goedert M. Alpha-synuclein and neurodegenerative diseases. Nat Rev Neurosci. 2001; 2: 492-501.
76. Tetzlaff JE, Putcha P, Outeiro TF, Ivanov A, Berezovska O, Hyman BT, McLean PJ. CHIP targets toxic alpha- Synuclein oligomers for degradation. J Biol Chem. 2008; 283: 17962-17968.
77. Kalia LV, Kalia SK, Chau H, Lozano AM, Hyman BT, McLean PJ. Ubiquitinylation of alpha-synuclein by carboxyl terminus Hsp70-interacting protein (CHIP) is regulated by Bcl-2-associated athanogene 5 (BAG5). PloS One. 2011; 6: e14695.
78. Imai Y, Soda M, Takahashi, R. Parkin suppresses unfolded protein stress-induced cell death through its E3 ubiquitinprotein ligase activity. J Biol Chem. 2000; 275: 35661- 35664.
79. Imai Y, Soda M, Inoue H, Hattori N, Mizuno Y, Takahashi R. An unfolded putative transmembrane polypeptide, which can lead to endoplasmic reticulum stress, is a substrate of Parkin. Cell. 2001; 105: 891-902.
80. Imai Y, Soda M, Hatakeyama S, Akagi T, Hashikawa T, Nakayama KI, Takahashi R. CHIP is associated with Parkin, a gene responsible for familial Parkinson's disease, and enhances its ubiquitin ligase activity. Mol Cell. 2002; 10: 55-67.
81. Hashimoto M, Rockenstein E, Crews L, Masliah E. Role of protein aggregation in mitochondrial dysfunction and neurodegeneration in Alzheimer's and Parkinson's diseases. Neuromolecular Med. 2003; 4: 21-36.
82. Kumar P, Ambasta RK, Veereshwarayya V, Rosen KM, Kosik KS, Band H, Mestril R, Patterson C, Querfurth HW. CHIP and HSPs interact with beta-APP in a proteasome-dependent manner and influence Abeta metabolism. Hum Mol Genet. 2007; 16: 848-864.
83. Wang JZ, Xia YY, Grundke-Iqbal I, Iqbal K. Abnormal hyperphosphorylation of tau: sites, regulation, and molecular mechanism of neurofibrillary degeneration. J Alzheimers Dis. 2013; 33 Suppl 1: S123-139.
84. Shimura H, Schwartz D, Gygi SP, Kosik KS. CHIP-Hsc70 complex ubiquitinates phosphorylated tau and enhances cell survival. J Biol Chem. 2004; 279: 4869-4876.
85. Hatakeyama S, Matsumoto M, Kamura T, Murayama M, Chui DH, Planel E, Takahashi R, Nakayama KI, Takashima A. U-box protein carboxyl terminus of Hsc70-interacting protein (CHIP) mediates polyubiquitylation preferentially on four-repeat Tau and is involved in neurodegeneration of tauopathy. J Neurochem. 2004; 91: 299-307.
86. Kojima Y, Miyoshi H, Clevers HC, Oshima M, Aoki M, Taketo MM. Suppression of tubulin polymerization by the LKB1-microtubule-associated protein/microtubule affinity-regulating kinase signaling. J Biol Chem. 2007; 282: 23532-23540.
87. Crow MT. Revisiting p53 and its effectors in ischemic heart injury. Cardiovascular research. 2006; 70(3):401-403.
88. Matsusaka H, Ide T, Matsushima S, Ikeuchi M, Kubota T, Sunagawa K, Kinugawa S and Tsutsui H. Targeted deletion of p53 prevents cardiac rupture after myocardial infarction in mice. Cardiovascular research. 2006; 70(3):457-465.
89. Naito AT, Okada S, Minamino T, Iwanaga K, Liu ML, Sumida T, Nomura S, Sahara N, Mizoroki T, Takashima A, Akazawa H, Nagai T, Shiojima I and Komuro I. Promotion of CHIP-mediated p53 degradation protects the heart from ischemic injury. Circulation research. 2010; 106(11):1692- 1702.
90. Woo CH, Le NT, Shishido T, Chang E, Lee H, Heo KS, Mickelsen DM, Lu Y, McClain C, Spangenberg T, Yan C, Molina CA, Yang J, Patterson C and Abe J. Novel role of C terminus of Hsc70-interacting protein (CHIP) ubiquitin ligase on inhibiting cardiac apoptosis and dysfunction via regulating ERK5-mediated degradation of inducible cAMP early repressor. FASEB journal. 2010; 24(12):4917-4928.
91. Yang K, Zhang TP, Tian C, Jia LX, Du J and Li HH. Carboxyl terminus of heat shock protein 70-interacting protein inhibits angiotensin II-induced cardiac remodeling. American journal of hypertension. 2012; 25(9):994-1001.