152
Views
3
CrossRef citations to date
0
Altmetric
Original Research

Single-Cell Sequencing to Identify Six Heat Shock Protein (HSP) Genes-Mediated Progression Subtypes of Clear Cell Renal Cell Carcinoma

, ORCID Icon, & ORCID Icon
Pages 3761-3773 | Published online: 23 Jul 2021

References

  • Turajlic S, Swanton C, Boshoff C. Kidney cancer: the next decade. J Exp Med. 2018;215(10):2477–2479. doi:10.1084/jem.20181617
  • Barata PC, Rini BI. Treatment of renal cell carcinoma: current status and future directions. CA Cancer J Clin. 2017;67(6):507–524. doi:10.3322/caac.21411
  • Störkel S, van den Berg E. Morphological classification of renal cancer. World J Urol. 1995;13(3):153–158. doi:10.1007/bf00184870
  • Srigley JR, Delahunt B, Eble JN, et al. The International Society of Urological Pathology (ISUP) vancouver classification of renal neoplasia. Am J Surg Pathol. 2013;37(10):1469–1489. doi:10.1097/PAS.0b013e318299f2d1
  • Nickerson ML, Jaeger E, Shi Y, et al. Improved identification of von Hippel-Lindau gene alterations in clear cell renal tumors. Clin Cancer Res. 2008;14(15):4726–4734. doi:10.1158/1078-0432.Ccr-07-4921
  • Team TACSmaec. American Cancer Society. Survival rates for kidney cancer. Available from: https://www.cancer.org/cancer/kidney-cancer/detection-diagnosis-staging/survival-rates.html#references. Accessed July 12, 2021.
  • Tsukimi Y, Okabe S. Recent advances in gastrointestinal pathophysiology: role of heat shock proteins in mucosal defense and ulcer healing. Biol Pharm Bull. 2001;24(1):1–9. doi:10.1248/bpb.24.1
  • Janowitz T, Welsh SJ, Zaki K, Mulders P, Eisen T. Adjuvant therapy in renal cell carcinoma-past, present, and future. Semin Oncol. 2013;40(4):482–491. doi:10.1053/j.seminoncol.2013.05.004
  • Stephenson AJ, Chetner MP, Rourke K, et al. Guidelines for the surveillance of localized renal cell carcinoma based on the patterns of relapse after nephrectomy. J Urol. 2004;172(1):58–62. doi:10.1097/01.ju.0000132126.85812.7d
  • Jäättelä M. Heat shock proteins as cellular lifeguards. Ann Med. 1999;31(4):261–271. doi:10.3109/07853899908995889
  • Jego G, Hazoumé A, Seigneuric R, Garrido C. Targeting heat shock proteins in cancer. Cancer Lett. 2013;332(2):275–285. doi:10.1016/j.canlet.2010.10.014
  • Wang X, Chen M, Zhou J, Zhang X. HSP27, 70 and 90, anti-apoptotic proteins, in clinical cancer therapy (Review). Int J Oncol. 2014;45(1):18–30. doi:10.3892/ijo.2014.2399
  • Wu J, Liu T, Rios Z, Mei Q, Lin X, Cao S. Heat shock proteins and cancer. Trends Pharmacol Sci. 2017;38(3):226–256. doi:10.1016/j.tips.2016.11.009
  • Ciocca DR, Calderwood SK. Heat shock proteins in cancer: diagnostic, prognostic, predictive, and treatment implications. Cell Stress Chaperones. 2005;10(2):86–103. doi:10.1379/csc-99r.1
  • Beere HM. The stress of dying”: the role of heat shock proteins in the regulation of apoptosis. J Cell Sci. 2004;117(Pt13):2641–2651. doi:10.1242/jcs.01284
  • Lindquist S, Craig EA. The heat-shock proteins. Annu Rev Genet. 1988;22:631–677. doi:10.1146/annurev.ge.22.120188.003215
  • Liu T, Daniels CK, Cao S. Comprehensive review on the HSC70 functions, interactions with related molecules and involvement in clinical diseases and therapeutic potential. Pharmacol Ther. 2012;136(3):354–374. doi:10.1016/j.pharmthera.2012.08.014
  • Macario AJ, Conway de macario E. Molecular chaperones: multiple functions, pathologies, and potential applications. Front Biosci. 2007;12:2588–2600. doi:10.2741/2257
  • Jolly C, Morimoto RI. Role of the heat shock response and molecular chaperones in oncogenesis and cell death. J Natl Cancer Inst. 2000;92(19):1564–1572. doi:10.1093/jnci/92.19.1564
  • Lianos GD, Alexiou GA, Mangano A, et al. The role of heat shock proteins in cancer. Cancer Lett. 2015;360(2):114–118. doi:10.1016/j.canlet.2015.02.026
  • Gething MJ, Sambrook J. Protein folding in the cell. Nature. 1992;355(6355):33–45. doi:10.1038/355033a0
  • Nollen EA, Morimoto RI. Chaperoning signaling pathways: molecular chaperones as stress-sensing ‘heat shock’ proteins. J Cell Sci. 2002;115(Pt 14):2809–2816.
  • Calderwood SK, Khaleque MA, Sawyer DB, Ciocca DR. Heat shock proteins in cancer: chaperones of tumorigenesis. Trends Biochem Sci. 2006;31(3):164–172. doi:10.1016/j.tibs.2006.01.006
  • Tsan MF, Gao B. Cytokine function of heat shock proteins. Am J Physiol Cell Physiol. 2004;286(4):C739–44. doi:10.1152/ajpcell.00364.2003
  • Das JK, Xiong X, Ren X, Yang JM, Song J. Heat shock proteins in cancer immunotherapy. J Oncol. 2019;2019:3267207. doi:10.1155/2019/3267207
  • Murshid A, Theriault J, Gong J, Calderwood SK. Investigating receptors for extracellular heat shock proteins. Methods Mol Biol. 2011;787:289–302. doi:10.1007/978-1-61779-295-3_22
  • González-Silva L, Quevedo L, Varela I. Tumor functional heterogeneity unraveled by scRNA-seq technologies. Trends Cancer. 2020;6(1):13–19. doi:10.1016/j.trecan.2019.11.010
  • Wu H, Humphreys BD. The promise of single-cell RNA sequencing for kidney disease investigation. Kidney Int. 2017;92(6):1334–1342. doi:10.1016/j.kint.2017.06.033
  • Mereu E, Lafzi A, Moutinho C, et al. Benchmarking single-cell RNA-sequencing protocols for cell atlas projects. Nat Biotechnol. 2020;38(6):747–755. doi:10.1038/s41587-020-0469-4
  • Navin NE. Cancer genomics: one cell at a time. Genome Biol. 2014;15(8):452. doi:10.1186/s13059-014-0452-9
  • Zheng GX, Terry JM, Belgrader P, et al. Massively parallel digital transcriptional profiling of single cells. Nat Commun. 2017;8:14049. doi:10.1038/ncomms14049
  • Kim KT, Lee HW, Lee HO, et al. Application of single-cell RNA sequencing in optimizing a combinatorial therapeutic strategy in metastatic renal cell carcinoma. Genome Biol. 2016;17:80. doi:10.1186/s13059-016-0945-9
  • Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15(12):550. doi:10.1186/s13059-014-0550-8
  • Yu G. Enrichplot: visualization of functional enrichment result. Available from: https://github.com/GuangchuangYu/enrichplot. Accessed July 12, 2021.
  • Szklarczyk D, Gable AL, Lyon D, et al. STRING v11: protein-protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets. Nucleic Acids Res. 2019;47(D1):D607–d613. doi:10.1093/nar/gky1131
  • Chin CH, Chen SH, Wu HH, Ho CW, Ko MT, Lin CY. cytoHubba: identifying hub objects and sub-networks from complex interactome. BMC Syst Biol. 2014;8(Suppl 4):S11. doi:10.1186/1752-0509-8-s4-s11
  • Shannon P, Markiel A, Ozier O, et al. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 2003;13(11):2498–2504. doi:10.1101/gr.1239303
  • Wilkerson MD, Hayes DN. ConsensusClusterPlus: a class discovery tool with confidence assessments and item tracking. Bioinformatics (Oxford, England). 2010;26(12):1572–1573. doi:10.1093/bioinformatics/btq170
  • Therneau TM. A Package for Survival Analysis in R; 2020. Therneau TM, Grambsch PM. Modeling Survival Data: Extending the Cox Model. Springer (New York).2000; ISBN:0-387-98784-3.
  • Li T, Fu J, Zeng Z, et al. TIMER2.0 for analysis of tumor-infiltrating immune cells. Nucleic Acids Res. 2020;48(W1):W509–w514. doi:10.1093/nar/gkaa407
  • Newman AM, Liu CL, Green MR, et al. Robust enumeration of cell subsets from tissue expression profiles. Nat Methods. 2015;12(5):453–457. doi:10.1038/nmeth.3337
  • Geeleher P, Cox N, Huang RS. pRRophetic: an R package for prediction of clinical chemotherapeutic response from tumor gene expression levels. PLoS One. 2014;9(9):e107468. doi:10.1371/journal.pone.0107468
  • Zhu Y, Cang S, Chen B, et al. Patient stratification of clear cell renal cell carcinoma using the global transcription factor activity landscape derived from RNA-Seq data. Front Oncol. 2020;10:526577. doi:10.3389/fonc.2020.526577
  • Zhong W, Zhang F, Huang C, Lin Y, Huang J. Classification of clear cell renal cell carcinoma based on tumor suppressor genomic profiling. J Cancer. 2021;12(8):2359–2370. doi:10.7150/jca.50462
  • Kosari F, Parker AS, Kube DM, et al. Clear cell renal cell carcinoma: gene expression analyses identify a potential signature for tumor aggressiveness. Clin Cancer Res. 2005;11(14):5128–5139. doi:10.1158/1078-0432.Ccr-05-0073
  • Gerlinger M, Rowan AJ, Horswell S, et al. Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. N Engl J Med. 2012;366(10):883–892. doi:10.1056/NEJMoa1113205
  • Potter SS. Single-cell RNA sequencing for the study of development, physiology and disease. Nat Rev Nephrol. 2018;14(8):479–492. doi:10.1038/s41581-018-0021-7
  • Wu B, Hunt C, Morimoto R. Structure and expression of the human gene encoding major heat shock protein HSP70. Mol Cell Biol. 1985;5(2):330–341. doi:10.1128/mcb.5.2.330
  • Milner CM, Campbell RD. Structure and expression of the three MHC-linked HSP70 genes. Immunogenetics. 1990;32(4):242–251. doi:10.1007/bf00187095
  • Murphy ME. The HSP70 family and cancer. Carcinogenesis. 2013;34(6):1181–1188. doi:10.1093/carcin/bgt111
  • Guo F, Sigua C, Bali P, et al. Mechanistic role of heat shock protein 70 in Bcr-Abl-mediated resistance to apoptosis in human acute leukemia cells. Blood. 2005;105(3):1246–1255. doi:10.1182/blood-2004-05-2041
  • Gabai VL, Yaglom JA, Waldman T, Sherman MY. Heat shock protein Hsp72 controls oncogene-induced senescence pathways in cancer cells. Mol Cell Biol. 2009;29(2):559–569. doi:10.1128/mcb.01041-08
  • Ramp U, Mahotka C, Heikaus S, et al. Expression of heat shock protein 70 in renal cell carcinoma and its relation to tumor progression and prognosis. Histol Histopathol. 2007;22(10):1099–1107. doi:10.14670/hh-22.1099
  • Sonna LA, Fujita J, Gaffin SL, Lilly CM. Invited review: effects of heat and cold stress on mammalian gene expression. J Appl Physiol. 2002;92(4):1725–1742. doi:10.1152/japplphysiol.01143.2001
  • Dworniczak B, Mirault ME. Structure and expression of a human gene coding for a 71 kd heat shock ‘cognate’ protein. Nucleic Acids Res. 1987;15(13):5181–5197. doi:10.1093/nar/15.13.5181
  • Rutherford SL, Zuker CS. Protein folding and the regulation of signaling pathways. Cell. 1994;79(7):1129–1132. doi:10.1016/0092-8674(94)90003-5
  • Shiota M, Kusakabe H, Izumi Y, et al. Heat shock cognate protein 70 is essential for Akt signaling in endothelial function. Arterioscler Thromb Vasc Biol. 2010;30(3):491–497. doi:10.1161/atvbaha.109.193631
  • Kubota H, Yamamoto S, Itoh E, et al. Increased expression of co-chaperone HOP with HSP90 and HSC70 and complex formation in human colonic carcinoma. Cell Stress Chaperones. 2010;15(6):1003–1011. doi:10.1007/s12192-010-0211-0
  • Helmbrecht K, Rensing L. Different constitutive heat shock protein 70 expression during proliferation and differentiation of rat C6 glioma cells. Neurochem Res. 1999;24(10):1293–1299. doi:10.1023/a:1020933308947
  • Azuma K, Shichijo S, Takedatsu H, Komatsu N, Sawamizu H, Itoh K. Heat shock cognate protein 70 encodes antigenic epitopes recognised by HLA-B4601-restricted cytotoxic T lymphocytes from cancer patients. Br J Cancer. 2003;89(6):1079–1085. doi:10.1038/sj.bjc.6601203
  • Yehiely F, Oren M. The gene for the rat heat-shock cognate, hsc70, can suppress oncogene-mediated transformation. Cell Growth Differentiation. 1992;3(11):803–809.
  • Ozawa K, Murakami Y, Eki T, Soeda E, Yokoyama K. Mapping of the gene family for human heat-shock protein 90 alpha to chromosomes 1, 4, 11, and 14. Genomics. 1992;12(2):214–220. doi:10.1016/0888-7543(92)90368-3
  • Zuehlke AD, Beebe K, Neckers L, Prince T. Regulation and function of the human HSP90AA1 gene. Gene. 2015;570(1):8–16. doi:10.1016/j.gene.2015.06.018
  • Jameel A, Skilton RA, Campbell TA, Chander SK, Coombes RC, Luqmani YA. Clinical and biological significance of HSP89 alpha in human breast cancer. Int J Cancer. 1992;50(3):409–415. doi:10.1002/ijc.2910500315
  • Gress TM, Müller-Pillasch F, Weber C, et al. Differential expression of heat shock proteins in pancreatic carcinoma. Cancer Res. 1994;54(2):547–551.
  • Teng SC, Chen YY, Su YN, et al. Direct activation of HSP90A transcription by c-Myc contributes to c-Myc-induced transformation. J Biol Chem. 2004;279(15):14649–14655. doi:10.1074/jbc.M308842200
  • Nonoguchi K, Tokuchi H, Okuno H, et al. Expression of Apg-1, a member of the Hsp110 family, in the human testis and sperm. Int J Urol. 2001;8(6):308–314. doi:10.1046/j.1442-2042.2001.00304.x
  • Hosaka S, Nakatsura T, Tsukamoto H, Hatayama T, Baba H, Nishimura Y. Synthetic small interfering RNA targeting heat shock protein 105 induces apoptosis of various cancer cells both in vitro and in vivo. Cancer Sci. 2006;97(7):623–632. doi:10.1111/j.1349-7006.2006.00217.x
  • Rauch JN, Gestwicki JE. Binding of human nucleotide exchange factors to heat shock protein 70 (Hsp70) generates functionally distinct complexes in vitro. J Biol Chem. 2014;289(3):1402–1414. doi:10.1074/jbc.M113.521997
  • Zappasodi R, Ruggiero G, Guarnotta C, et al. HSPH1 inhibition downregulates Bcl-6 and c-Myc and hampers the growth of human aggressive B-cell non-Hodgkin lymphoma. Blood. 2015;125(11):1768–1771. doi:10.1182/blood-2014-07-590034
  • Zhang K, Jiang K, Hong R, et al. Identification and characterization of critical genes associated with tamoxifen resistance in breast cancer. Peer J. 2020;8:e10468. doi:10.7717/peerj.10468