Cited by 145Cancer, Lipids, and MetabolismCholesterol and Lipid MetabolismSphingolipid Metabolism and Signaling

Apolipoproteins and cancer

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Ren, Liwen, Yi, Jie, Li, Wan, Zheng, Xiangjin, Liu, Jinyi, Wang, Jinhua, Du, Guanhua·2019·Cancer Medicine

Abstract

The role of apolipoproteins in cardiovascular disease has been well investigated, but their participation in cancer has only been explored in a few published studies which showed a close link with certain kinds of cancer. In this review, we focused on the function of different kinds of apolipoproteins in cancers, autophagy, oxidative stress, and drug resistance. The potential application of apolipoproteins as biomarkers for cancer diagnosis and prognosis was highlighted, together with an investigation of their potential as drug targets for cancer treatment. Many important roles of apolipoproteins and their mechanisms in cancers were reviewed in detail and future perspectives of apolipoprotein research were discussed.

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  1. [2]Emerging Risk Factors C, Di Angelantonio E, Sarwar N, et al. Major lipids, apolipoproteins, and risk of vascular disease. JAMA. 2009; 302: 1993‐ 2000. 19903920 PMC3284229
  2. [3]von Zychlinski A, Williams M, McCormick S, Kleffmann T. Absolute quantification of apolipoproteins and associated proteins on human plasma lipoproteins. J Proteomics. 2014; 106: 181‐ 190. 24780726
  3. [4]Marcil V, Delvin E, Seidman E, et al. Modulation of lipid synthesis, apolipoprotein biogenesis, and lipoprotein assembly by butyrate. Am J Physiol Gastrointest Liver Physiol. 2002; 283: G340‐ G346. 12121881
  4. [6]Su F, Lang J, Kumar A, et al. Validation of candidate serum ovarian cancer biomarkers for early detection. Biomark Insights. 2007; 2: 369‐ 375. 19662218 PMC2717832
  5. [7]Shi H, Huang H, Pu J, et al. Decreased pretherapy serum apolipoprotein A‐I is associated with extent of metastasis and poor prognosis of non‐small‐cell lung cancer. Onco Targets Ther. 2018; 11: 6995‐ 7003. 30410356 PMC6199218
  6. [8]Luo X‐L, Zhong G‐Z, Hu L‐Y, et al. Serum apolipoprotein A‐I is a novel prognostic indicator for non‐metastatic nasopharyngeal carcinoma. Oncotarget. 2015; 6: 44037‐ 44048. 26503474 PMC4791285
  7. [9]Quan QI, Huang Y, Chen QI, et al. Impact of serum apolipoprotein A‐I on prognosis and bevacizumab efficacy in patients with metastatic colorectal cancer: a propensity score‐matched analysis. Transl Oncol. 2017; 10: 288‐ 294. 28292509 PMC5334545
  8. [10]Quan Q, Chen Q, Chen P, et al. Decreased apolipoprotein A‐I level indicates poor prognosis in extranodal natural killer/t‐cell lymphoma, nasal type. Onco Targets Ther. 2016; 9: 1281‐ 1290. 27051293 PMC4803244
  9. [11]Van Hemelrijck M, Walldius G, Jungner I, et al. Low levels of apolipoprotein A‐I and HDL are associated with risk of prostate cancer in the swedish amoris study. Cancer Causes Control. 2011; 22: 1011‐ 1019. 21562751
  10. [12]Guo S, He X, Chen Q, et al. The effect of preoperative apolipoprotein A‐I on the prognosis of surgical renal cell carcinoma: a retrospective large sample study. Medicine. 2016; 95: e3147. 27015197 PMC4998392
  11. [13]Shi J, Yang H, Duan X, et al. Apolipoproteins as differentiating and predictive markers for assessing clinical outcomes in patients with small cell lung cancer. Yonsei Med J. 2016; 57: 549‐ 556. 26996551 PMC4800341
  12. [14]Bharali D, Banerjee BD, Bharadwaj M, Husain SA, Kar P. Expression analysis of apolipoproteins AI & AIV in hepatocellular carcinoma: a protein‐based hepatocellular carcinoma‐associated study. Indian J Med Res. 2018; 147: 361‐ 368. 29998871 PMC6057253
  13. [15]Ma XL, Gao XH, Gong ZJ, et al. Apolipoprotein A1: a novel serum biomarker for predicting the prognosis of hepatocellular carcinoma after curative resection. Oncotarget. 2016; 7: 70654‐ 70668. 27683106 PMC5342581
  14. [16]Li C, Li H, Zhang T, Li J, Liu L, Chang J. Discovery of APO‐A1 as a potential bladder cancer biomarker by urine proteomics and analysis. Biochem Biophys Res Commun. 2014; 446: 1047‐ 1052. 24661883
  15. [17]Shang Z, Wang J, Wang X, et al. Preoperative serum apolipoprotein A‐I levels predict long‐term survival in non‐muscle‐invasive bladder cancer patients. Cancer Manag Res. 2018; 10: 1177‐ 1190. 29795989 PMC5958942
  16. [18]Lin X, Hong S, Huang J, Chen Y, Chen Y, Wu Z. Plasma apolipoprotein A1 levels at diagnosis are independent prognostic factors in invasive ductal breast cancer. Discov Med. 2017; 23: 247‐ 258. 28595037
  17. [19]Chang S‐J, Hou M‐F, Tsai S‐M, et al. The association between lipid profiles and breast cancer among taiwanese women. Clin Chem Lab Med. 2007; 45: 1219‐ 1223. 17663634
  18. [20]Kim BK, Lee JW, Park PJ, et al. The multiplex bead array approach to identifying serum biomarkers associated with breast cancer. Breast Cancer Res. 2009; 11: R22. 19400944 PMC2688951
  19. [21]Cedó L, Reddy ST, Mato E, Blanco‐Vaca F, Escolà‐Gil JC. HDL and LDL: potential new players in breast cancer development. J Clin Med. 2019; 8(6): 853. PMC6616617 31208017
  20. [22]Reddy ST, Navab M, Anantharamaiah GM, Fogelman AM. Apolipoprotein A‐I mimetics. Curr Opin Lipidol. 2014; 25: 304‐ 308. 24977978 PMC4213064
  21. [23]Su F, Kozak KR, Imaizumi S, et al. Apolipoprotein A‐I (apoA‐I) and apoA‐I mimetic peptides inhibit tumor development in a mouse model of ovarian cancer. Proc Natl Acad Sci USA. 2010; 107: 19997‐ 20002. 21041624 PMC2993420
  22. [24]Cedó L, García‐León A, Baila‐Rueda L, et al. ApoA‐I mimetic administration, but not increased apoA‐I‐containing HDL, inhibits tumour growth in a mouse model of inherited breast cancer. Sci Rep. 2016; 6: 36387. 27808249 PMC5093413
  23. [25]Su F, Grijalva V, Navab K, et al. HDL mimetics inhibit tumor development in both induced and spontaneous mouse models of colon cancer. Mol Cancer Ther. 2012; 11: 1311‐ 1319. 22416044 PMC3374063
  24. [26]Peng M, Zhang QI, Cheng Y, et al. Apolipoprotein A‐I mimetic peptide 4f suppresses tumor‐associated macrophages and pancreatic cancer progression. Oncotarget. 2017; 8: 99693‐ 99706. 29245934 PMC5725125
  25. [27]Zamanian‐Daryoush M, Lindner D, Tallant TC, et al. The cardioprotective protein apolipoprotein A1 promotes potent anti‐tumorigenic effects. J Biol Chem. 2013; 288: 21237‐ 21252. 23720750 PMC3774392
  26. [28]Gkouskou KK, Ioannou M, Pavlopoulos GA, et al. Apolipoprotein A‐I inhibits experimental colitis and colitis‐propelled carcinogenesis. Oncogene. 2016; 35: 2496‐ 2505. 26279300
  27. [29]Hachem H, Favre G, Ghalim N, Puchois P, Fruchart JC, Soula G. Quantitative abnormalities of lipoprotein particles in multiple myeloma. J Clin Chem Clin Biochem. 1987; 25: 675‐ 679. 3121778
  28. [30]Humphries JM, Penno M, Weiland F, et al. Identification and validation of novel candidate protein biomarkers for the detection of human gastric cancer. Biochim Biophys Acta. 2014; 1844: 1051‐ 1058. 24512919
  29. [31]Liu Y, Sogawa K, Sunaga M, et al. Increased concentrations of Apo A‐I and Apo A‐II fragments in the serum of patients with hepatocellular carcinoma by magnetic beads‐assisted maldi‐tof mass spectrometry. Am J Clin Pathol. 2014; 141: 52‐ 61. 24343737
  30. [32]Malik G, Ward MD, Gupta SK, et al. Serum levels of an isoform of apolipoprotein A‐II as a potential marker for prostate cancer. Clin Cancer Res. 2005; 11: 1073‐ 1085. 15709174
  31. [33]de Bont JM, den Boer ML, Reddingius RE, et al. Identification of apolipoprotein A‐II in cerebrospinal fluid of pediatric brain tumor patients by protein expression profiling. Clin Chem. 2006; 52: 1501‐ 1509. 16762995
  32. [34]Honda K, Kobayashi M, Okusaka T, et al. Plasma biomarker for detection of early stage pancreatic cancer and risk factors for pancreatic malignancy using antibodies for apolipoprotein‐aii isoforms. Sci Rep. 2015; 5: 15921. 26549697 PMC4637825
  33. [35]Dieplinger H, Ankerst DP, Burges A, et al. Afamin and apolipoprotein A‐IV: novel protein markers for ovarian cancer. Cancer Epidemiol Biomarkers Prev. 2009; 18: 1127‐ 1133. 19336561
  34. [36]Lee G, Jeong YS, Kim DW, et al. Clinical significance of APOB inactivation in hepatocellular carcinoma. Exp Mol Med. 2018; 50: 147. 30429453 PMC6235894
  35. [37]Mahley RW, Innerarity TL, Rall SC Jr, Weisgraber KH. Plasma lipoproteins: Apolipoprotein structure and function. J Lipid Res. 1984; 25: 1277‐ 1294. 6099394
  36. [38]Takano S, Yoshitomi H, Togawa A, et al. Apolipoprotein C‐1 maintains cell survival by preventing from apoptosis in pancreatic cancer cells. Oncogene. 2008; 27: 2810‐ 2822. 18037960
  37. [39]Song D, Yue L, Zhang J, et al. Diagnostic and prognostic significance of serum apolipoprotein C‐I in triple‐negative breast cancer based on mass spectrometry. Cancer Biol Ther. 2016; 17: 635‐ 647. 27260686 PMC4990397
  38. [40]Yang X, Lu B, Sun X, et al. ANP32A regulates histone H3 acetylation and promotes leukemogenesis. Leukemia. 2018; 32: 1587‐ 1597. 29467488
  39. [41]Klee EW, Bondar OP, Goodmanson MK, et al. Candidate serum biomarkers for prostate adenocarcinoma identified by mrna differences in prostate tissue and verified with protein measurements in tissue and blood. Clin Chem. 2012; 58: 599‐ 609. 22247499 PMC3951013
  40. [42]Ko HL, Wang YS, Fong WL, Chi MS, Chi KH, Kao SJ. Apolipoprotein C1 (APOC1) as a novel diagnostic and prognostic biomarker for lung cancer: a marker phase I trial. Thorac Cancer. 2014; 5: 500‐ 508. 26767044 PMC4704334
  41. [43]Yang Y, Zhao S, Fan Y, et al. Detection and identification of potential biomarkers of non‐small cell lung cancer. Technol Cancer Res Treat. 2009; 8: 455‐ 466. 19925029
  42. [44]Engwegen JY, Depla AC, Smits ME, et al. Detection of colorectal cancer by serum and tissue protein profiling: a prospective study in a population at risk. Biomark Insights. 2008; 3: 375‐ 385. 19578519 PMC2688344
  43. [45]Fan Y, Shi L, Liu Q, et al. Discovery and identification of potential biomarkers of papillary thyroid carcinoma. Mol Cancer. 2009; 8: 79. 19785722 PMC2761863
  44. [46]Zhang J, Guo F, Wang L, et al. Identification of apolipoprotein C‐I as a potential wilms' tumor marker after excluding inflammatory factors. Int J Mol Sci. 2014; 15: 16186‐ 16195. 25222555 PMC4200791
  45. [47]Ren H, Chen Z, Yang L, et al. Apolipoprotein C1 (APOC1) promotes tumor progression via mapk signaling pathways in colorectal cancer. Cancer Manag Res. 2019; 11: 4917‐ 4930. 31213910 PMC6549782
  46. [48]Xue A, Chang JW, Chung L, et al. Serum apolipoprotein C‐II is prognostic for survival after pancreatic resection for adenocarcinoma. Br J Cancer. 2012; 107: 1883‐ 1891. 23169340 PMC3504954
  47. [49]Rassart E, Bedirian A, Do Carmo S, et al. Apolipoprotein D. Biochim Biophys Acta. 2000; 1482: 185‐ 198. 11058760
  48. [50]Utsunomiya T, Ogawa K, Yoshinaga K, et al. Clinicopathologic and prognostic values of apolipoprotein d alterations in hepatocellular carcinoma. Int J Cancer. 2005; 116: 105‐ 109. 15756681
  49. [51]Ogawa K, Utsunomiya T, Mimori K, et al. Genomic screens for genes upregulated by demethylation in colorectal cancer: possible usefulness for clinical application. Int J Oncol. 2005; 27: 417‐ 426. 16010423
  50. [52]Vazquez J, Gonzalez L, Merino A, Vizoso F. Expression and clinical significance of apolipoprotein d in epithelial ovarian carcinomas. Gynecol Oncol. 2000; 76: 340‐ 347. 10684708
  51. [53]Hunter S, Young A, Olson J, et al. Differential expression between pilocytic and anaplastic astrocytomas: Identification of apolipoprotein D as a marker for low‐grade, non‐infiltrating primary CNS neoplasms. J Neuropathol Exp Neurol. 2002; 61: 275‐ 281. 11895042
  52. [54]Diez‐Itza I, Vizoso F, Merino AM, et al. Expression and prognostic significance of apolipoprotein d in breast cancer. Am J Pathol. 1994; 144: 310‐ 320. 8311115 PMC1887137
  53. [55]Miranda E, Vizoso F, Martín A, et al. Apolipoprotein D expression in cutaneous malignant melanoma. J Surg Oncol. 2003; 83: 99‐ 105. 12772203
  54. [56]Hall RE, Horsfall DJ, Stahl J, et al. Apolipoprotein‐D: a novel cellular marker for HGPIN and prostate cancer. Prostate. 2004; 58: 103‐ 108. 14716735
  55. [57]Sandim V, Pereira D, Kalume DE, et al. Proteomic analysis reveals differentially secreted proteins in the urine from patients with clear cell renal cell carcinoma. Urol Oncol. 2016; 34(5): e11‐ 25. 26420021
  56. [58]Huebbe P, Rimbach G. Evolution of human apolipoprotein E (APOE) isoforms: Gene structure, protein function and interaction with dietary factors. Ageing Res Rev. 2017; 37: 146‐ 161. 28647612
  57. [59]Trost Z, Marc J, Sok M, Cerne D. Increased apolipoprotein E gene expression and protein concentration in lung cancer tissue do not contribute to the clinical assessment of non‐small cell lung cancer patients. Arch Med Res. 2008; 39: 663‐ 667. 18760194
  58. [60]Luo J, Song J, Feng P, et al. Elevated serum apolipoprotein E is associated with metastasis and poor prognosis of non‐small cell lung cancer. Tumour Biol. 2016; 37: 10715‐ 10721. 26873483
  59. [61]Sakashita K, Tanaka F, Zhang X, et al. Clinical significance of APOE expression in human gastric cancer. Oncol Rep. 2008; 20: 1313‐ 1319. 19020708
  60. [62]Oue N, Hamai Y, Mitani Y, et al. Gene expression profile of gastric carcinoma: Identification of genes and tags potentially involved in invasion, metastasis, and carcinogenesis by serial analysis of gene expression. Cancer Res. 2004; 64: 2397‐ 2405. 15059891
  61. [63]Chen YC, Pohl G, Wang TL, et al. Apolipoprotein E is required for cell proliferation and survival in ovarian cancer. Cancer Res. 2005; 65: 331‐ 337. 15665311
  62. [64]Kim Y‐W, Bae SM, Kim I‐W, et al. Multiplexed bead‐based immunoassay of four serum biomarkers for diagnosis of ovarian cancer. Oncol Rep. 2012; 28: 585‐ 591. 22641176
  63. [65]Venanzoni M, Giunta S, Muraro G, et al. Apolipoprotein E expression in localized prostate cancers. Int J Oncol. 2003; 22: 779‐ 786. 12632068
  64. [66]Martin P, Noonan S, Mullen MP, et al. Predicting response to vascular endothelial growth factor inhibitor and chemotherapy in metastatic colorectal cancer. BMC Cancer. 2014; 14: 887. 25428203 PMC4289341
  65. [67]Lindén M, Segersten U, Runeson M, et al. Tumour expression of bladder cancer‐associated urinary proteins. BJU Int. 2013; 112: 407‐ 415. 23470167
  66. [68]Urquidi V, Goodison S, Ross S, Chang M, Dai Y, Rosser CJ. Diagnostic potential of urinary alpha1‐antitrypsin and apolipoprotein E in the detection of bladder cancer. J Urol. 2012; 188: 2377‐ 2383. 23088986 PMC4013779
  67. [69]Chen J, Chen L‐J, Yang R‐B, et al. Expression and clinical significance of apolipoprotein E in pancreatic ductal adenocarcinoma. Med Oncol. 2013; 30: 583. 23609192
  68. [70]Xu X, Wan J, Yuan L, et al. Serum levels of apolipoprotein E correlates with disease progression and poor prognosis in breast cancer. Tumour Biol. 2016; 37(12): 15959‐ 15966. 27709551
  69. [71]Yokoyama Y, Kuramitsu Y, Takashima M, et al. Protein level of apolipoprotein E increased in human hepatocellular carcinoma. Int J Oncol. 2006; 28: 625‐ 631. 16465366
  70. [72]Nicoll JA, Zunarelli E, Rampling R, Murray LS, Papanastassiou V, Stewart J. Involvement of apolipoprotein E in glioblastoma: immunohistochemistry and clinical outcome. NeuroReport. 2003; 14: 1923‐ 1926. 14561921
  71. [74]Pencheva N, Tran H, Buss C, et al. Convergent multi‐miRNA targeting of ApoE drives LRP1/LRP8‐dependent melanoma metastasis and angiogenesis. Cell. 2012; 151: 1068‐ 1082. 23142051 PMC3753115
  72. [75]Borchman D, Harris EN, Pierangeli SS, Lamba OP. Interactions and molecular structure of cardiolipin and beta 2‐glycoprotein 1 (beta 2‐GP1). Clin Exp Immunol. 1995; 102: 373‐ 378. 7586693 PMC1553418
  73. [76]Jing X, Piao YF, Liu Y, Gao PJ. Beta2‐GPI: a novel factor in the development of hepatocellular carcinoma. J Cancer Res Clin Oncol. 2010; 136: 1671‐ 1680. 20204408 PMC11828206
  74. [77]Mandili G, Notarpietro A, Khadjavi A, et al. Beta‐2‐glycoprotein‐1 and alpha‐1‐antitrypsin as urinary markers of renal cancer in von hippel‐lindau patients. Biomarkers. 2018; 23: 123‐ 130. 28004973
  75. [78]Lee S‐W, Kim IJ, Jeong BY, et al. Use of MDLC‐DIGE and LC‐MS/MS to identify serum biomarkers for complete remission in patients with acute myeloid leukemia. Electrophoresis. 2012; 33: 1863‐ 1872. 22740475
  76. [79]Vanhollebeke B, Pays E. The function of apolipoproteins L. Cell Mol Life Sci. 2006; 63: 1937‐ 1944. 16847577 PMC11136045
  77. [80]Chidiac M, Fayyad‐Kazan M, Daher J, et al. Apolipoproteinl1 is expressed in papillary thyroid carcinomas. Pathol Res Pract. 2016; 212: 631‐ 635. 27157405
  78. [81]Chu J, Li N, Li F. A risk score staging system based on the expression of seven genes predicts the outcome of bladder cancer. Oncol Lett. 2018; 16: 2091‐ 2096. 30008905 PMC6036497
  79. [82]Johanneson B, McDonnell SK, Karyadi DM, et al. Family‐based association analysis of 42 hereditary prostate cancer families identifies the apolipoprotein L3 region on chromosome 22q12 as a risk locus. Hum Mol Genet. 2010; 19: 3852‐ 3862. 20631155 PMC2935853
  80. [83]Liu Z, Lu H, Jiang Z, Pastuszyn A, Hu CA. Apolipoprotein L6, a novel proapoptotic BCL‐2 homology 3‐only protein, induces mitochondria‐mediated apoptosis in cancer cells. Mol Cancer Res. 2005; 3: 21‐ 31. 15671246
  81. [84]Zhu Y, Luo G, Jiang BO, et al. Apolipoprotein M promotes proliferation and invasion in non‐small cell lung cancers via upregulating S1PR1 and activating the ERK1/2 and PI3K/AKT signaling pathways. Biochem Biophys Res Commun. 2018; 501: 520‐ 526. 29750961
  82. [85]Jiang J, Wu C, Luo G, et al. Expression of apolipoprotein M in human hepatocellular carcinoma tissues. Acta Histochem. 2011; 113: 53‐ 57. 19796793
  83. [86]Hu Y‐W, Chen Z‐P, Hu X‐M, et al. The miR‐573/apoM/Bcl2A1‐dependent signal transduction pathway is essential for hepatocyte apoptosis and hepatocarcinogenesis. Apoptosis. 2015; 20: 1321‐ 1337. 26201458
  84. [87]Luo G, Zhang X, Mu Q, et al. Expression and localization of apolipoprotein m in human colorectal tissues. Lipids Health Dis. 2010; 9: 102. 20846402 PMC2945960
  85. [88]Trougakos IP, Gonos ES. Clusterin/apolipoprotein J in human aging and cancer. Int J Biochem Cell Biol. 2002; 34: 1430‐ 1448. 12200037
  86. [89]Tellez T, Garcia‐Aranda M, Redondo M. The role of clusterin in carcinogenesis and its potential utility as therapeutic target. Curr Med Chem. 2016; 23: 4297‐ 4308. 27781946
  87. [90]Trougakos IP, So A, Jansen B, Gleave ME, Gonos ES. Silencing expression of the clusterin/apolipoprotein J gene in human cancer cells using small interfering RNA induces spontaneous apoptosis, reduced growth ability, and cell sensitization to genotoxic and oxidative stress. Cancer Res. 2004; 64: 1834‐ 1842. 14996747
  88. [91]Chi KN, Eisenhauer E, Fazli L, et al. A phase I pharmacokinetic and pharmacodynamic study of OGX‐011, a 2'‐methoxyethyl antisense oligonucleotide to clusterin, in patients with localized prostate cancer. J Natl Cancer Inst. 2005; 97: 1287‐ 1296. 16145049
  89. [92]Saad F, Hotte S, North S, et al. Randomized phase II trial of custirsen (OGX‐011) in combination with docetaxel or mitoxantrone as second‐line therapy in patients with metastatic castrate‐resistant prostate cancer progressing after first‐line docetaxel: Cuog trial P‐06c. Clin Cancer Res. 2011; 17: 5765‐ 5773. 21788353
  90. [93]Miyake H, Muramaki M, Kurahashi T, et al. Expression of clusterin in prostate cancer correlates with gleason score but not with prognosis in patients undergoing radical prostatectomy without neoadjuvant hormonal therapy. Urology. 2006; 68: 609‐ 614. 16979705
  91. [94]Kang YK, Hong SW, Lee H, Kim WH. Overexpression of clusterin in human hepatocellular carcinoma. Hum Pathol. 2004; 35: 1340‐ 1346. 15668890
  92. [95]Wang C, Jiang K, Kang X, et al. Tumor‐derived secretory clusterin induces epithelial‐mesenchymal transition and facilitates hepatocellular carcinoma metastasis. Int J Biochem Cell Biol. 2012; 44: 2308‐ 2320. 23010347
  93. [96]Xiu P, Xu Z, Liu F, et al. Downregulating sclu enhances the sensitivity of hepatocellular carcinoma cells to gemcitabine by activating the intrinsic apoptosis pathway. Dig Dis Sci. 2014; 59: 1798‐ 1809. 24671452
  94. [97]Xie D, Sham JS, Zeng WF, et al. Oncogenic role of clusterin overexpression in multistage colorectal tumorigenesis and progression. World J Gastroenterol. 2005; 11: 3285‐ 3289. 15929184 PMC4316065
  95. [98]Redondo M, Rodrigo I, Alcaide J, et al. Clusterin expression is associated with decreased disease‐free survival of patients with colorectal carcinomas. Histopathology. 2010; 56: 932‐ 936. 20497247
  96. [99]Bertuzzi M, Marelli C, Bagnati R, et al. Plasma clusterin as a candidate pre‐diagnosis marker of colorectal cancer risk in the florence cohort of the european prospective investigation into cancer and nutrition: a pilot study. BMC Cancer. 2015; 15: 56. 25884309 PMC4334607
  97. [100]Pucci S, Bonanno E, Pichiorri F, Angeloni C, Spagnoli LG. Modulation of different clusterin isoforms in human colon tumorigenesis. Oncogene. 2004; 23: 2298‐ 2304. 14755245
  98. [101]Gunawardana CG, Kuk C, Smith CR, Batruch I, Soosaipillai A, Diamandis EP. Comprehensive analysis of conditioned media from ovarian cancer cell lines identifies novel candidate markers of epithelial ovarian cancer. J Proteome Res. 2009; 8: 4705‐ 4713. 19663500
  99. [102]Yang GF, Li XM, Xie D. Overexpression of clusterin in ovarian cancer is correlated with impaired survival. Int J Gynecol Cancer. 2009; 19: 1342‐ 1346. 20009887
  100. [103]Lyu N, Wang Y, Wang J, Zhang Z, Kong W. Study on early diagnosis of epithelial ovarian cancer by analysis of plasma septin‐9 and clusterin level. J Cancer Res Ther. 2018; 14: S444‐ S449. 29970704
  101. [104]Redondo M, Villar E, Torres‐Munoz J, Tellez T, Morell M, Petito CK. Overexpression of clusterin in human breast carcinoma. Am J Pathol. 2000; 157: 393‐ 399. 10934144 PMC1850123
  102. [105]Yom CK, Woo HY, Min SY, Kang SY, Kim HS. Clusterin overexpression and relapse‐free survival in breast cancer. Anticancer Res. 2009; 29: 3909‐ 3912. 19846927
  103. [106]Li J, Jia L, Zhao P, Jiang Y, Zhong S, Chen D. Stable knockdown of clusterin by vectorbased rna interference in a human breast cancer cell line inhibits tumour cell invasion and metastasis. J Int Med Res. 2012; 40: 545‐ 555. 22613415
  104. [107]Miyake H, Hara S, Arakawa S, Kamidono S, Hara I. Over expression of clusterin is an independent prognostic factor for nonpapillary renal cell carcinoma. J Urol. 2002; 167: 703‐ 706. 11792957
  105. [108]Vange P, Bruland T, Doseth B, et al. The cytoprotective protein clusterin is overexpressed in hypergastrinemic rodent models of oxyntic preneoplasia and promotes gastric cancer cell survival. PLoS ONE. 2017; 12: e0184514. 28902909 PMC5597207
  106. [109]Jin J, Kim J‐M, Hur Y‐S, et al. Clinical significance of clusterin expression in pancreatic adenocarcinoma. World J Surg Oncol. 2012; 10: 146. 22799602 PMC3436747
  107. [110]Albert JM, Gonzalez A, Massion PP, et al. Cytoplasmic clusterin expression is associated with longer survival in patients with resected non small cell lung cancer. Cancer Epidemiol Biomarkers Prev. 2007; 16: 1845‐ 1851. 17855704
  108. [111]Shapiro B, Tocci P, Haase G, Gavert N, Ben‐Ze'ev A. Clusterin, a gene enriched in intestinal stem cells, is required for L1‐mediated colon cancer metastasis. Oncotarget. 2015; 6: 34389‐ 34401. 26399194 PMC4741460
  109. [112]Radziwon‐Balicka A, Santos‐Martinez MJ, Corbalan JJ, et al. Mechanisms of platelet‐stimulated colon cancer invasion: Role of clusterin and thrombospondin 1 in regulation of the P38MAPK‐MMP‐9 pathway. Carcinogenesis. 2014; 35: 324‐ 332. 24085798
  110. [113]Wang Y, Wang X, Zhao H, Liang B, Du Q. Clusterin confers resistance to TNF‐alpha‐induced apoptosis in breast cancer cells through NF‐kappaB activation and BCL‐2 overexpression. J Chemother. 2012; 24: 348‐ 357. 23174100
  111. [114]Mathew R, Karantza‐Wadsworth V, White E. Role of autophagy in cancer. Nat Rev Cancer. 2007; 7: 961‐ 967. 17972889 PMC2866167
  112. [115]Fulda S. Autophagy in cancer therapy. Front Oncol. 2017; 7: 128. 28674677 PMC5475391
  113. [116]Mowers EE, Sharifi MN, Macleod KF. Autophagy in cancer metastasis. Oncogene. 2017; 36: 1619‐ 1630. 27593926 PMC5337449
  114. [117]Sui X, Chen R, Wang Z, et al. Autophagy and chemotherapy resistance: a promising therapeutic target for cancer treatment. Cell Death Dis. 2013; 4: e838. 24113172 PMC3824660
  115. [121]Ginsberg HN, Fisher EA. The ever‐expanding role of degradation in the regulation of apolipoprotein b metabolism. J Lipid Res. 2009; 50(Suppl): S162‐ S166. 19050312 PMC2674708
  116. [122]Conlon DM, Thomas T, Fedotova T, et al. Inhibition of apolipoprotein B synthesis stimulates endoplasmic reticulum autophagy that prevents steatosis. J Clin Invest. 2016; 126: 3852‐ 3867. 27599291 PMC5096813
  117. [123]Parcon PA, Balasubramaniam M, Ayyadevara S, et al. Apolipoprotein E4 inhibits autophagy gene products through direct, specific binding to clear motifs. Alzheimers Dement. 2018; 14: 230‐ 242. 28945989 PMC6613789
  118. [124]Wan G, Zhaorigetu S, Liu Z, Kaini R, Jiang Z, Hu CA. Apolipoprotein L1, a novel BCL‐2 homology domain 3‐only lipid‐binding protein, induces autophagic cell death. J Biol Chem. 2008; 283: 21540‐ 21549. 18505729 PMC2490785
  119. [125]Zhaorigetu S, Yang Z, Toma I, McCaffrey TA, Hu CA. Apolipoprotein L6, induced in atherosclerotic lesions, promotes apoptosis and blocks beclin 1‐dependent autophagy in atherosclerotic cells. J Biol Chem. 2011; 286: 27389‐ 27398. 21646352 PMC3149332
  120. [126]Wang B, Feng D, Han L, et al. Combination of apolipoprotein A1‐modi liposome‐doxorubicin with autophagy inhibitors overcame drug resistance in vitro. J Pharm Sci. 2014; 103: 3994‐ 4004. 25354472
  121. [127]Morry J, Ngamcherdtrakul W, Yantasee W. Oxidative stress in cancer and fibrosis: opportunity for therapeutic intervention with antioxidant compounds, enzymes, and nanoparticles. Redox Biol. 2017; 11: 240‐ 253. 28012439 PMC5198743
  122. [128]Galaris D, Skiada V, Barbouti A. Redox signaling and cancer: the role of "labile" iron. Cancer Lett. 2008; 266: 21‐ 29. 18374479
  123. [129]Pani G, Galeotti T, Chiarugi P. Metastasis: cancer cell's escape from oxidative stress. Cancer Metastasis Rev. 2010; 29: 351‐ 378. 20386957
  124. [130]Bajo‐Grañeras R, Crespo‐Sanjuan J, García‐Centeno RM, et al. Expression and potential role of apolipoprotein D on the death‐survival balance of human colorectal cancer cells under oxidative stress conditions. Int J Colorectal Dis. 2013; 28: 751‐ 766. 23296401
  125. [131]Yiu CC, Sasano H, Ono K, Chow LW. Changes in protein expression after neoadjuvant use of aromatase inhibitors in primary breast cancer: a proteomic approach to search for potential biomarkers to predict response or resistance. Expert Opin Investig Drugs. 2010; 19(Suppl 1): S79‐ 89. 20374034
  126. [132]Cruz IN, Coley HM, Kramer HB, et al. Proteomics analysis of ovarian cancer cell lines and tissues reveals drug resistance‐associated proteins. Cancer Genomics Proteomics. 2017; 14: 35‐ 51. 28031236 PMC5267499
  127. [133]Soiland H, Skaland I, Varhaug JE, et al. Co‐expression of estrogen receptor alpha and apolipoprotein D in node positive operable breast cancer–possible relevance for survival and effects of adjuvant tamoxifen in postmenopausal patients. Acta Oncol. 2009; 48: 514‐ 521. 19107621
  128. [134]Liu M, Feng LX, Sun P, et al. Knockdown of apolipoprotein E enhanced sensitivity of HEP3B cells to cardiac steroids via regulating na+/k+‐ATPASE signalosome. Mol Cancer Ther. 2016; 15: 2955‐ 2965. 27507851
  129. [135]Gleave ME, Miyake H, Zellweger T, et al. Use of antisense oligonucleotides targeting the antiapoptotic gene, clusterin/testosterone‐repressed prostate message 2, to enhance androgen sensitivity and chemosensitivity in prostate cancer. Urology. 2001; 58: 39‐ 49. 11502446
  130. [136]Chun YJ. Knockdown of clusterin expression increases the in vitro sensitivity of human prostate cancer cells to paclitaxel. J Toxicol Environ Health A. 2014; 77: 1443‐ 1450. 25343293
  131. [137]Zellweger T, Chi K, Miyake H, et al. Enhanced radiation sensitivity in prostate cancer by inhibition of the cell survival protein clusterin. Clin Cancer Res. 2002; 8: 3276‐ 3284. 12374699
  132. [138]Muramaki M, So A, Hayashi N, et al. Chemosensitization of gemcitabine‐resistant human bladder cancer cell line both in vitro and in vivo using antisense oligonucleotide targeting the anti‐apoptotic gene, clusterin. BJU Int. 2009; 103: 384‐ 390. 19007378
  133. [139]Wang X, Luo L, Dong D, Yu Q, Zhao K. Clusterin plays an important role in clear renal cell cancer metastasis. Urol Int. 2014; 92: 95‐ 103. 24008723
  134. [140]Lee C‐H, Jin RJ, Kwak C, et al. Suppression of clusterin expression enhanced cisplatin‐induced cytotoxicity on renal cell carcinoma cells. Urology. 2002; 60: 516‐ 520. 12350509
  135. [141]Kususda Y, Miyake H, Gleave ME, Fujisawa M. Clusterin inhibition using OGX‐011 synergistically enhances antitumour activity of sorafenib in a human renal cell carcinoma model. Br J Cancer. 2012; 106: 1945‐ 1952. 22588555 PMC3388571
  136. [142]Chen Q, Wang Z, Zhang K, et al. Clusterin confers gemcitabine resistance in pancreatic cancer. World J Surg Oncol. 2011; 9: 59. 21609464 PMC3120680
  137. [143]Tang Y, Liu F, Zheng C, Sun S, Jiang Y. Knockdown of clusterin sensitizes pancreatic cancer cells to gemcitabine chemotherapy by ERK1/2 inactivation. J Exp Clin Cancer Res. 2012; 31: 73. 22967941 PMC3561651
  138. [144]Park DC, Yeo SG, Shin EY, Mok SC, Kim DH. Clusterin confers paclitaxel resistance in cervical cancer. Gynecol Oncol. 2006; 103: 996‐ 1000. 16890274
  139. [145]Lourda M, Trougakos IP, Gonos ES. Development of resistance to chemotherapeutic drugs in human osteosarcoma cell lines largely depends on up‐regulation of clusterin/apolipoprotein J. Int J Cancer. 2007; 120: 611‐ 622. 17096323
  140. [146]Sung H, Siegel RL, Torre LA, et al. Global patterns in excess body weight and the associated cancer burden. CA Cancer J Clin. 2018; 69: 88‐ 112. 30548482
  141. [147]Calle EE, Thun MJ. Obesity and cancer. Oncogene. 2004; 23: 6365‐ 6378. 15322511

Cited by

Sorted by citations

Authors
Ren, L., Yi, J., Li, W., Zheng, X., Liu, J., Wang, J., & Du, G.
Affiliations
  • Chinese Academy of Medical Sciences & Peking Union Medical College (CN)
  • Peking Union Medical College Hospital (CN)
Corresponding author
  • Wang, Jinhua
  • Du, Guanhua
Venue
Cancer Medicine
Publisher
Wiley
Published
2019-10
Volume
8
Issue
16
Pages
7032-7043
ISSN
2045-7634 (ISSN-L)
OpenAlex
W2978056808
Cited by
145
References
6
Citations by year
2026: 14 · 2025: 24 · 2024: 26 · 2023: 21 · 2022: 21 · 2021: 30 · 2020: 8 · 2019: 1
FWCI
1.44
Type
journal article
Language
en
Open access
Locations
  • Cancer Medicine (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • Natural Science Foundation of Beijing Municipality (7172142)
  • National Natural Science Foundation of China (81573454)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Lipids, and Metabolism
  • Health Sciences › Medicine › Surgery › Cholesterol and Lipid Metabolism
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Sphingolipid Metabolism and Signaling
Keywords
apolipoproteins, cancer, autophagy, oxidative stress, drug resistance, tumor markers, cancer diagnosis and prognosis, therapeutic target, cardiovascular disease
MeSH terms
Animals, Apolipoproteins, Autophagy, Humans, Neoplasms, Oxidative Stress, Drug Resistance, Neoplasm

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