Abstract
As an extension of their orchestration of intracellular pathways, secretion of extracellular heat shock proteins (HSPs) is an emerging paradigm of homeostasis imperative to multicellular organization. Extracellular HSP is axiomatic to the survival of cells during tumorigenesis; proportional representation of specific HSP family members is indicative of invasive potential and prognosis. Further significance has been added by the knowledge that all cancer-derived exosomes have surface-exposed HSPs that reflect the membrane topology of cells that secrete them. Extracellular HSPs are also characteristic of chronic inflammation and sepsis. Accordingly, interrogation of extracellular HSPs secreted from cell culture models may represent a facile means of identifying translational biomarker signatures for targeting in situ. In the current study, we evaluated a simple peptide-based multivalent HSP affinity approach using the Vn96 peptide for low speed pelleting of HSP complexes from bioreactor cultures of cell lines with varying invasive phenotype in xenotransplant models: U87 (glioblastoma multiforme; invasive); HELA (choriocarcinoma; minimally invasive); HEK293T (virally transformed immortalized; embryonic). Proteomic profiling by bottom-up mass spectrometry revealed a comprehensive range of candidate biomarkers including primary HSP ligands. HSP complexes were associated with additional chaperones of prognostic significance such as protein disulfide isomerases, as well as pleiotropic metabolic enzymes, established as proportionally reflective of invasive phenotype. Biomarkers of inflammatory and mechanotransductive phenotype were restricted to the most invasive cell model U87, including chitinase CHI3L1, lamin C, amyloid derivatives, and histone isoforms.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Change history
23 December 2020
A Correction to this paper has been published: <ExternalRef><RefSource>https://doi.org/10.1007/s12192-020-01187-w</RefSource><RefTarget Address="10.1007/s12192-020-01187-w" TargetType="DOI"/></ExternalRef>
References
Bhatia A, O’Brien K, Chen M et al (2016) Keratinocyte-secreted heat shock protein-90alpha: Leading wound reepithelialization and closure. Adv Wound Care 5:176–184. https://doi.org/10.1089/wound.2014.0620
Bijnsdorp IV, Maxouri O, Kardar A, Schelfhorst T, Piersma SR, Pham TV, Vis A, van Moorselaar R, Jimenez CR (2017) Feasibility of urinary extracellular vesicle proteome profiling using a robust and simple, clinically applicable isolation method. J Extracell Vesicles 6:1313091. https://doi.org/10.1080/20013078.2017.1313091
Brehme M, Voisine C, Rolland T, Wachi S, Soper JH, Zhu Y, Orton K, Villella A, Garza D, Vidal M, Ge H, Morimoto RI (2014) A chaperome subnetwork safeguards proteostasis in aging and neurodegenerative disease. Cell Rep 9:1135–1150. https://doi.org/10.1016/j.celrep.2014.09.042
Briassouli E, Goukos D, Daikos G, Apostolou K, Routsi C, Nanas S, Briassoulis G (2014) Glutamine suppresses Hsp72 not Hsp90α and is not inducing Th1, Th2, or Th17 cytokine responses in human septic PBMCs. Nutrition 30:1185–1194. https://doi.org/10.1016/j.nut.2014.01.018
Briassouli E, Tzanoudaki M, Goukos D et al (2015) Glutamine may repress the weak LPS and enhance the strong heat shock induction of monocyte and lymphocyte HSP72 proteins but may not modulate the HSP72 mRNA in patients with sepsis or trauma. Biomed Res Int 2015:1–15. https://doi.org/10.1155/2015/806042
Briassoulis G, Briassouli E, Fitrolaki D-M, Plati I, Apostolou K, Tavladaki T, Spanaki AM (2014) Heat shock protein 72 expressing stress in sepsis: unbridgeable gap between animal and human studies--a hypothetical “comparative” study. Biomed Res Int 2014:101023. https://doi.org/10.1155/2014/101023
Briassoulis G, Briassoulis P, Miliaraki M, Ilia S, Parlato M, Philippart F, Rouquette A, Moucadel V, Cavaillon JM, Misset B, Combined Approach for The eArly diagnosis of INfection in sepsis (CAPTAIN) study group (2019) Biomarker cruises in sepsis: who is the CAPTAIN? Discussion on “Circulating biomarkers may be unable to detect infection at the early phase of sepsis in ICU patients: the CAPTAIN prospective multicenter cohort study”. Intensive Care Med 45:132–133. https://doi.org/10.1007/s00134-018-5451-y
Calderwood SK, Murshid A, Gong J (2012) heat shock proteins: conditional mediators of inflammation in tumor immunity. Front Immunol 3:75. https://doi.org/10.3389/fimmu.2012.00075
Capello M, Ferri-Borgogno S, Riganti C et al (2016) Targeting the Warburg effect in cancer cells through ENO1 knockdown rescues oxidative phosphorylation and induces growth arrest. Oncotarget 7:5598–5612. https://doi.org/10.18632/oncotarget.6798
Caruso Bavisotto C, Graziano F, Rappa F et al (2018) Exosomal chaperones and miRNAs in gliomagenesis: state-of-art and theranostics perspectives. Int J Mol Sci 19:2626. https://doi.org/10.3390/ijms19092626
Castillo J, Bernard V, San Lucas FA, Allenson K, Capello M, Kim DU, Gascoyne P, Mulu FC, Stephens BM, Huang J, Wang H, Momin AA, Jacamo RO, Katz M, Wolff R, Javle M, Varadhachary G, Wistuba II, Hanash S, Maitra A, Alvarez H (2018) Surfaceome profiling enables isolation of cancer-specific exosomal cargo in liquid biopsies from pancreatic cancer patients. Ann Oncol 29:223–229. https://doi.org/10.1093/annonc/mdx542
Cavassani KA, Meza RJ, Habiel DM, Chen JF, Montes A, Tripathi M, Martins GA, Crother TR, You S, Hogaboam CM, Bhowmick N, Posadas EM (2018) Circulating monocytes from prostate cancer patients promote invasion and motility of epithelial cells. Cancer Med 7:4639–4649. https://doi.org/10.1002/cam4.1695
Chaitanya G, Alexander JS, Babu P (2010) PARP-1 cleavage fragments: signatures of cell-death proteases in neurodegeneration. Cell Commun Signal 8:31. https://doi.org/10.1186/1478-811X-8-31
Chatterjee N, Chatterjee A (2001) Role of alphavbeta3 integrin receptor in the invasive potential of human cervical cancer (SiHa) cells. J Environ Pathol Toxicol Oncol 20:211–221
Chen S-T, Pan T-L, Juan H-F, Chen TY, Lin YS, Huang CM (2008) Breast tumor microenvironment: proteomics highlights the treatments targeting secretome. J Proteome Res 7:1379–1387. https://doi.org/10.1021/pr700745n
Chen R, Kang R, Fan X-G, Tang D (2014) Release and activity of histone in diseases. Cell Death Dis 5:e1370–e1370. https://doi.org/10.1038/cddis.2014.337
Chen H-T, Zheng J-M, Zhang Y-Z, Yang M, Wang YL, Man XH, Chen Y, Cai QC, Li ZS (2017a) Overexpression of YKL-40 predicts poor prognosis in patients undergoing curative resection of pancreatic cancer. Pancreas 46:323–334. https://doi.org/10.1097/MPA.0000000000000751
Chen Y, Zhang S, Wang Q, Zhang X (2017b) Tumor-recruited M2 macrophages promote gastric and breast cancer metastasis via M2 macrophage-secreted CHI3L1 protein. J Hematol Oncol 10:36. https://doi.org/10.1186/s13045-017-0408-0
Chen Y, Wang H, Tan C, Yan Y, Shen J, Huang Q, Xu T, Lin J, Chen J (2018) Expression of amyloid precursor-like protein 2 (APLP2) in glioblastoma is associated with patient prognosis. Folia Neuropathol 56:30–38. https://doi.org/10.5114/fn.2018.74657
Chiang Y-C, Lin H-W, Chang C-F et al (2015) Overexpression of CHI3L1 is associated with chemoresistance and poor outcome of epithelial ovarian carcinoma. Oncotarget 6:39740–39755. https://doi.org/10.18632/oncotarget.5469
Cohen N, Shani O, Raz Y, Sharon Y, Hoffman D, Abramovitz L, Erez N (2017) Fibroblasts drive an immunosuppressive and growth-promoting microenvironment in breast cancer via secretion of Chitinase 3-like 1. Oncogene 36:4457–4468. https://doi.org/10.1038/onc.2017.65
Crouch B, Murphy H, Belonwu S, Martinez A, Gallagher J, Hall A, Soo MS, Lee M, Hughes P, Haystead T, Ramanujam N (2017) Leveraging ectopic Hsp90 expression to assay the presence of tumor cells and aggressive tumor phenotypes in breast specimens. Sci Rep 7:17487. https://doi.org/10.1038/s41598-017-17832-x
Crowe LB, Hughes PF, Alcorta DA, Osada T, Smith AP, Totzke J, Loiselle DR, Lutz ID, Gargesha M, Roy D, Roques J, Darr D, Lyerly HK, Spector NL, Haystead TAJ (2017) A fluorescent Hsp90 probe demonstrates the unique association between extracellular Hsp90 and malignancy in vivo. ACS Chem Biol 12:1047–1055. https://doi.org/10.1021/acschembio.7b00006
Cui Y, Niu M, Zhang X, Zhong Z, Wang J, Pang D (2015) High expression of valosin-containing protein predicts poor prognosis in patients with breast carcinoma. Tumor Biol 36:9919–9927. https://doi.org/10.1007/s13277-015-3748-9
Dai J, Ji Y, Wang W, Kim D, Fai LY, Wang L, Luo J, Zhang Z (2017) Loss of fructose-1,6-bisphosphatase induces glycolysis and promotes apoptosis resistance of cancer stem-like cells: an important role in hexavalent chromium-induced carcinogenesis. Toxicol Appl Pharmacol 331:164–173. https://doi.org/10.1016/j.taap.2017.06.014
De Maio A, Vazquez D (2013) Extracellular heat shock proteins: a new location, a new function. Shock 40:239–246. https://doi.org/10.1097/SHK.0b013e3182a185ab
Debeb BG, Zhang X, Krishnamurthy S, Gao H, Cohen E, Li L, Rodriguez AA, Landis MD, Lucci A, Ueno NT, Robertson F, Xu W, Lacerda L, Buchholz TA, Cristofanilli M, Reuben JM, Lewis MT, Woodward WA (2010) Characterizing cancer cells with cancer stem cell-like features in 293T human embryonic kidney cells. Mol Cancer 9:180. https://doi.org/10.1186/1476-4598-9-180
Diamandis EP (2012) The failure of protein cancer biomarkers to reach the clinic: why, and what can be done to address the problem? BMC Med 10:87. https://doi.org/10.1186/1741-7015-10-87
Dong G, Mao Q, Xia W, Xu Y, Wang J, Xu L, Jiang F (2016) PKM2 and cancer: the function of PKM2 beyond glycolysis. Oncol Lett 11:1980–1986. https://doi.org/10.3892/ol.2016.4168
Duriez PJ, Shah GM (1997) Cleavage of poly(ADP-ribose) polymerase: a sensitive parameter to study cell death. Biochem Cell Biol 75:337–349
Edkins AL, Price JT, Pockley AG, Blatch GL (2018) Heat shock proteins as modulators and therapeutic targets of chronic disease: an integrated perspective. Philos Trans R Soc B Biol Sci 373:20160521. https://doi.org/10.1098/rstb.2016.0521
Fitrolaki MD, Dimitriou H, Venihaki M, Katrinaki M, Ilia S, Briassoulis G (2016) Increased extracellular heat shock protein 90α in severe sepsis and SIRS associated with multiple organ failure and related to acute inflammatory-metabolic stress response in children. Medicine (Baltimore) 95:e4651. https://doi.org/10.1097/MD.0000000000004651
Fu Q, Jiang Y, Zhang D, Liu X, Guo J, Zhao J (2016) Valosin-containing protein (VCP) promotes the growth, invasion, and metastasis of colorectal cancer through activation of STAT3 signaling. Mol Cell Biochem 418:189–198. https://doi.org/10.1007/s11010-016-2746-6
Gandhi P, Khare R, VasudevGulwani H, Kaur S (2018) Circulatory YKL-40 & NLR: underestimated prognostic indicators in diffuse glioma. Int J Mol Cell Med 7:111–118. https://doi.org/10.22088/IJMCM.BUMS.7.2.111
Gastpar R, Gehrmann M, Bausero MA, Asea A, Gross C, Schroeder JA, Multhoff G (2005) Heat shock protein 70 surface-positive tumor exosomes stimulate migratory and cytolytic activity of natural killer cells. Cancer Res 65:5238–5247. https://doi.org/10.1158/0008-5472.CAN-04-3804
Ghaderi S, Ahmadian S, Soheili Z-S, Ahmadieh H, Samiei S, Kheitan S, Pirmardan ER (2018) AAV delivery of GRP78/BiP promotes adaptation of human RPE cell to ER stress. J Cell Biochem 119:1355–1367. https://doi.org/10.1002/jcb.26296
Ghosh A, Davey M, Chute IC, Griffiths SG, Lewis S, Chacko S, Barnett D, Crapoulet N, Fournier S, Joy A, Caissie MC, Ferguson AD, Daigle M, Meli MV, Lewis SM, Ouellette RJ (2014) Rapid isolation of extracellular vesicles from cell culture and biological fluids using a synthetic peptide with specific affinity for heat shock proteins. PLoS One 9:e110443. https://doi.org/10.1371/journal.pone.0110443
Gober MD, Wales SQ, Aurelian L (2005) Herpes simplex virus type 2 encodes a heat shock protein homologue with apoptosis regulatory functions. Front Biosci. 10:2788–2803
Gobbo J, Marcion G, Cordonnier M et al (2016) Restoring anticancer immune response by targeting tumor-derived exosomes with a HSP70 peptide aptamer. J Natl Cancer Inst 108:djv330. https://doi.org/10.1093/jnci/djv330
González-Cruz RD, Dahl KN, Darling EM (2018) The emerging role of lamin C as an important LMNA isoform in mechanophenotype. Front Cell Dev Biol 6:151. https://doi.org/10.3389/fcell.2018.00151
Grandjean G, de Jong PR, James BP, Koh MY, Lemos R, Kingston J, Aleshin A, Bankston LA, Miller CP, Cho EJ, Edupuganti R, Devkota A, Stancu G, Liddington RC, Dalby K, Powis G (2016) Definition of a novel feed-forward mechanism for glycolysis-HIF1α signaling in hypoxic tumors highlights aldolase A as a therapeutic target. Cancer Res 76:4259–4269. https://doi.org/10.1158/0008-5472.CAN-16-0401
Griffiths S, Lewis S, Belkaid A et al (2011) Peptides with affinity for cell-derived vesicles, presented at: First International Workshop on Exosomes, Paris, France, January 19-22.
Griffiths S, Cormier M, Clayton A, Doucette A (2017) Differential proteome analysis of extracellular vesicles from breast cancer cell lines by chaperone affinity enrichment. Proteomes 5:25. https://doi.org/10.3390/proteomes5040025
Gugliotta G, Sudo M, Cao Q, Lin DC, Sun H, Takao S, le Moigne R, Rolfe M, Gery S, Müschen M, Cavo M, Koeffler HP (2017) Valosin-containing protein/p97 as a novel therapeutic target in acute lymphoblastic leukemia. Neoplasia 19:750–761. https://doi.org/10.1016/j.neo.2017.08.001
Hadizadeh Esfahani A, Sverchkova A, Saez-Rodriguez J, Schuppert AA, Brehme M (2018) A systematic atlas of chaperome deregulation topologies across the human cancer landscape. PLoS Comput Biol 14:e1005890. https://doi.org/10.1371/journal.pcbi.1005890
Hall S, Janelidze S, Surova Y, Widner H, Zetterberg H, Hansson O (2018) Cerebrospinal fluid concentrations of inflammatory markers in Parkinson’s disease and atypical parkinsonian disorders. Sci Rep 8:13276. https://doi.org/10.1038/s41598-018-31517-z
Hamilton G, Rath B, Burghuber O (2015) Chitinase-3-like-1/YKL-40 as marker of circulating tumor cells. Transl Lung Cancer Res 4:287–291. https://doi.org/10.3978/j.issn.2218-6751.2015.04.04
Hariton-Gazal E, Rosenbluh J, Graessmann A, Gilon C, Loyter A (2003) Direct translocation of histone molecules across cell membranes. J Cell Sci 116:4577–4586. https://doi.org/10.1242/jcs.00757
Jeet V, Tevz G, Lehman M, Hollier B, Nelson C (2014) Elevated YKL40 is associated with advanced prostate cancer (PCa) and positively regulates invasion and migration of PCa cells. Endocr Relat Cancer 21:723–737. https://doi.org/10.1530/ERC-14-0267
Jeffery CJ (2018) Protein moonlighting: what is it, and why is it important? Philos Trans R Soc B Biol Sci 373:20160523. https://doi.org/10.1098/rstb.2016.0523
Jiang P, Gan M, Yen S-H, McLean P, Dickson DW (2017) Histones facilitate α-synuclein aggregation during neuronal apoptosis. Acta Neuropathol 133:547–558. https://doi.org/10.1007/s00401-016-1660-z
Jurisic V, Radenkovic S, Konjevic G (2015) The actual role of LDH as tumor marker, biochemical and clinical aspects. Adv Exp Med Biol 867:115–124. https://doi.org/10.1007/978-94-017-7215-0_8
Kakkar V, Meister-Broekema M, Minoia M, Carra S, Kampinga HH (2014) Barcoding heat shock proteins to human diseases: looking beyond the heat shock response. Dis Model Mech 7:421–434. https://doi.org/10.1242/dmm.014563
Kato J, Svensson CI (2015) Role of extracellular damage-associated molecular pattern molecules (damps) as mediators of persistent pain. Prog Mol Biol Transl Sci 131:251–279. https://doi.org/10.1016/bs.pmbts.2014.11.014
Khan IU, Wallin R, Gupta RS, Kammer GM (1998) Protein kinase A-catalyzed phosphorylation of heat shock protein 60 chaperone regulates its attachment to histone 2B in the T lymphocyte plasma membrane. Proc Natl Acad Sci U S A 95:10425–10430. https://doi.org/10.1073/pnas.95.18.10425
Khandia R, Munjal AK, Iqbal HMN, Dhama K (2017) Heat shock proteins: therapeutic perspectives in inflammatory disorders. Recent Patents Inflamm Allergy Drug Discov 10:94–104. https://doi.org/10.2174/1872213X10666161213163301
Klinke DJ (2016) Eavesdropping on altered cell-to-cell signaling in cancer by secretome profiling. Mol Cell Oncol 3:e1029061. https://doi.org/10.1080/23723556.2015.1029061
Klinke DJ, Kulkarni YM, Wu Y, Byrne-Hoffman C (2014) Inferring alterations in cell-to-cell communication in HER2+ breast cancer using secretome profiling of three cell models. Biotechnol Bioeng 111:1853–1863. https://doi.org/10.1002/bit.25238
Knol JC, de Reus I, Schelfhorst T, Beekhof R, de Wit M, Piersma SR, Pham TV, Smit EF, Verheul HMW, Jiménez CR (2016) Peptide-mediated ‘miniprep’ isolation of extracellular vesicles is suitable for high-throughput proteomics. EuPA Open Proteomics 11:11–15. https://doi.org/10.1016/j.euprot.2016.02.001
Kobiyama K, Kawashima A, Jounai N, Takeshita F, Ishii KJ, Ito T, Suzuki K (2013) Role of extrachromosomal histone H2B on recognition of DNA viruses and cell damage. Front Genet 4:91. https://doi.org/10.3389/fgene.2013.00091
Kuo LJ, Yang L-X (2008) Gamma-H2AX - a novel biomarker for DNA double-strand breaks. In Vivo 22:305–309
Lee E, Lee DH (2017) Emerging roles of protein disulfide isomerase in cancer. BMB Rep 50:401–410. https://doi.org/10.5483/bmbrep.2017.50.8.107
Libreros S, Iragavarapu-Charyulu V (2015) YKL-40/CHI3L1 drives inflammation on the road of tumor progression. J Leukoc Biol 98:931–936. https://doi.org/10.1189/jlb.3VMR0415-142R
Lim S, Yoo BK, Kim H-S, Gilmore HL, Lee Y, Lee HP, Kim SJ, Letterio J, Lee HG (2014) Amyloid-β precursor protein promotes cell proliferation and motility of advanced breast cancer. BMC Cancer 14:928. https://doi.org/10.1186/1471-2407-14-928
Liu H, Sadygov R, Yates J (2004) A model for random sampling and estimation of relative protein abundance in shotgun proteomics. Anal Chem 76:4193–4201. https://doi.org/10.1021/AC0498563
Llorens F, Thüne K, Tahir W, Kanata E, Diaz-Lucena D, Xanthopoulos K, Kovatsi E, Pleschka C, Garcia-Esparcia P, Schmitz M, Ozbay D, Correia S, Correia Â, Milosevic I, Andréoletti O, Fernández-Borges N, Vorberg IM, Glatzel M, Sklaviadis T, Torres JM, Krasemann S, Sánchez-Valle R, Ferrer I, Zerr I (2017) YKL-40 in the brain and cerebrospinal fluid of neurodegenerative dementias. Mol Neurodegener 12:83. https://doi.org/10.1186/s13024-017-0226-4
Marsman G, Zeerleder S, Luken BM (2016) Extracellular histones, cell-free DNA, or nucleosomes: differences in immunostimulation. Cell Death Dis 7:e2518. https://doi.org/10.1038/cddis.2016.410
Min K-W, Lee S-H, Baek SJ (2016) Moonlighting proteins in cancer. Cancer Lett 370:108–116. https://doi.org/10.1016/j.canlet.2015.09.022
Moir RD, Lathe R, Tanzi RE (2018) The antimicrobial protection hypothesis of Alzheimer’s disease. Alzheimers Dement 14:1602–1614. https://doi.org/10.1016/j.jalz.2018.06.3040
Neckers L, Blagg B, Haystead T, Trepel JB, Whitesell L, Picard D (2018) Methods to validate Hsp90 inhibitor specificity, to identify off-target effects, and to rethink approaches for further clinical development. Cell Stress Chaperones 23:467–482. https://doi.org/10.1007/s12192-018-0877-2
Niforou K, Cheimonidou C, Trougakos IP (2014) Molecular chaperones and proteostasis regulation during redox imbalance. Redox Biol 2:323–332. https://doi.org/10.1016/j.redox.2014.01.017
O’Brien K, Bhatia A, Tsen F et al (2014) Identification of the critical therapeutic entity in secreted Hsp90α that promotes wound healing in newly re-standardized healthy and diabetic pig models. PLoS One 9:e113956. https://doi.org/10.1371/journal.pone.0113956
Orton DJ, Doucette AA (2013) A universal, high recovery assay for protein quantitation through temperature programmed liquid chromatography (TPLC). J Chromatogr B Anal Technol Biomed Life Sci 921–922. https://doi.org/10.1016/j.jchromb.2013.01.021
Østergaard O, Nielsen CT, Tanassi JT, Iversen LV, Jacobsen S, Heegaard NHH (2017) Distinct proteome pathology of circulating microparticles in systemic lupus erythematosus. Clin Proteomics 14:23–13. https://doi.org/10.1186/s12014-017-9159-8
Palla V-V, Karaolanis G, Katafigiotis I et al (2017) gamma-H2AX: can it be established as a classical cancer prognostic factor? Tumor Biol 39:101042831769593. https://doi.org/10.1177/1010428317695931
Palotai R, Szalay MS, Csermely P (2007) Chaperones as integrators of cellular networks: changes of cellular integrity in stress and diseases. IUBMB Life 60:10–18. https://doi.org/10.1002/iub.8
Pandey P, Sliker B, Peters HL et al (2016) Amyloid precursor protein and amyloid precursor-like protein 2 in cancer. Oncotarget 7:19430–19444. https://doi.org/10.18632/oncotarget.7103
Papadopoulos P, Pistiki A, Theodorakopoulou M, Christodoulopoulou T, Damoraki G, Goukos D, Briassouli E, Dimopoulou I, Armaganidis A, Nanas S, Briassoulis G, Tsiodras S (2017) Immunoparalysis: clinical and immunological associations in SIRS and severe sepsis patients. Cytokine 92:83–92. https://doi.org/10.1016/j.cyto.2017.01.012
Parseghian MH, Luhrs KA (2006) Beyond the walls of the nucleus: the role of histones in cellular signaling and innate immunity. Biochem Cell Biol 84:589–595. https://doi.org/10.1139/o06-082
Perrucci GL, Gowran A, Zanobini M et al (2015) Peptidyl-prolyl isomerases: a full cast of critical actors in cardiovascular diseases. Cardiovasc Res 106:353–364. https://doi.org/10.1093/cvr/cvv096
Plesca D, Mazumder S, Almasan A (2008) DNA damage response and apoptosis. Methods Enzymol 446:107–122. https://doi.org/10.1016/S0076-6879(08)01606-6
Principe M, Ceruti P, Shih N-Y et al (2015) Targeting of surface alpha-enolase inhibits the invasiveness of pancreatic cancer cells. Oncotarget 6:11098–11113. https://doi.org/10.18632/oncotarget.3572
Ramsby ML, Makowski GS (1999) Differential detergent fractionation of eukaryotic cells: analysis by two-dimensional gel electrophoresis. In: 2-D proteome analysis protocols. Humana Press, Totowa, pp 53–66. https://doi.org/10.1385/1-59259-584-7:53
Rodvold JJ, Chiu KT, Hiramatsu N et al (2017) Intercellular transmission of the unfolded protein response promotes survival and drug resistance in cancer cells. Sci Signal 10:eaah7177. https://doi.org/10.1126/scisignal.aah7177
Ściborski K, Kuliczkowski W, Karolko B et al (2018) Plasma level of YKL-40 correlates with the severity of coronary atherosclerosis assessed with SYNTAX score. Polish Arch Intern Med 128:644–648. https://doi.org/10.20452/pamw.4345
Sharma A, Singh K, Almasan A (2012) Histone H2AX phosphorylation: a marker for DNA damage. Methods Mol Biol 920:613–626. https://doi.org/10.1007/978-1-61779-998-3_40
Shevchenko A, Tomas H, Havli J et al (2006) In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat Protoc 1:2856–2860. https://doi.org/10.1038/nprot.2006.468
Shevtsov M, Huile G, Multhoff G (2018) Membrane heat shock protein 70: a theranostic target for cancer therapy. Philos Trans R Soc B Biol Sci 373:20160526. https://doi.org/10.1098/rstb.2016.0526
Sirover MA (2018) Pleiotropic effects of moonlighting glyceraldehyde-3-phosphate dehydrogenase (GAPDH) in cancer progression, invasiveness, and metastases. Cancer Metastasis Rev 37:665–676. https://doi.org/10.1007/s10555-018-9764-7
Snaebjornsson MT, Schulze A (2018) Non-canonical functions of enzymes facilitate cross-talk between cell metabolic and regulatory pathways. Exp Mol Med 50:34. https://doi.org/10.1038/s12276-018-0065-6
Steiner N, Borjan B, Hajek R et al (2017) Expression and release of glucose-regulated protein-78 (GRP78) in multiple myeloma. Oncotarget 8:56243–56254. https://doi.org/10.18632/oncotarget.17353
Stifani S (2018) The multiple roles of peptidyl prolyl isomerases in brain cancer. Biomolecules 8:112. https://doi.org/10.3390/biom8040112
Strojnik T, Duh D, Lah TT (2017) Prevalence of neurotropic viruses in malignant glioma and their onco-modulatory potential. In Vivo (Brooklyn) 31:221–230. https://doi.org/10.21873/invivo.11049
Szatmary P, Huang W, Criddle D, Tepikin A, Sutton R (2018) Biology, role and therapeutic potential of circulating histones in acute inflammatory disorders. J Cell Mol Med 22:4617–4629. https://doi.org/10.1111/jcmm.13797
Tai W, Guzman ML, Chiosis G (2016) The epichaperome: the power of many as the power of one. Oncoscience 3:266. https://doi.org/10.18632/oncoscience.321
Thomaidou S, Zaldumbide A, Roep BO (2018) Islet stress, degradation and autoimmunity. Diabetes Obes Metab 20:88–94. https://doi.org/10.1111/dom.13387
Ucker DS, Jain MR, Pattabiraman G, Palasiewicz K, Birge RB, Li H (2012) Externalized glycolytic enzymes are novel, conserved, and early biomarkers of apoptosis. J Biol Chem 287:10325–10343. https://doi.org/10.1074/jbc.M111.314971
Vardas K, Apostolou K, Briassouli E, Goukos D, Psarra K, Botoula E, Tsagarakis S, Magira E, Routsi C, Nanas S, Briassoulis G (2014) Early response roles for prolactin cortisol and circulating and cellular levels of heat shock proteins 72 and 90α in severe sepsis and SIRS. Biomed Res Int 2014:803561. https://doi.org/10.1155/2014/803561
Vardas K, Ilia S, Sertedaki A, Charmandari E, Briassouli E, Goukos D, Apostolou K, Psarra K, Botoula E, Tsagarakis S, Magira E, Routsi C, Stratakis CA, Nanas S, Briassoulis G (2017) Increased glucocorticoid receptor expression in sepsis is related to heat shock proteins, cytokines, and cortisol and is associated with increased mortality. Intensive Care Med Exp 5:10. https://doi.org/10.1186/s40635-017-0123-8
Vekaria PH, Home T, Weir S et al (2016) Targeting p97 to disrupt protein homeostasis in cancer. Front Oncol 6:181. https://doi.org/10.3389/fonc.2016.00181
Wang X, Venable J, LaPointe P, Hutt DM, Koulov AV, Coppinger J, Gurkan C, Kellner W, Matteson J, Plutner H, Riordan JR, Kelly JW, Yates JR 3rd, Balch WE (2006) Hsp90 cochaperone Aha1 downregulation rescues misfolding of cftr in cystic fibrosis. Cell 127:803–815. https://doi.org/10.1016/j.cell.2006.09.043
Wang J, Ying G, Wang J, Jung Y, Lu J, Zhu J, Pienta KJ, Taichman RS (2010) Characterization of phosphoglycerate kinase-1 expression of stromal cells derived from tumor microenvironment in prostate cancer progression. Cancer Res 70:471–480. https://doi.org/10.1158/0008-5472.CAN-09-2863
Wang J, Lv H, Luo Z, Mou S, Liu J, Liu C, Deng S, Jiang Y, Lin J, Wu C, Liu X, He J, Jiang D (2018) Plasma YKL-40 and NGAL are useful in distinguishing ACO from asthma and COPD. Respir Res 19:47. https://doi.org/10.1186/s12931-018-0755-6
Wang T, Rodina A, Dunphy MP, Corben A, Modi S, Guzman ML, Gewirth DT, Chiosis G (2019) Chaperome heterogeneity and its implications for cancer study and treatment. J Biol Chem 294:2162–2179. https://doi.org/10.1074/jbc.REV118.002811
Wubbolts R, Leckie RS, Veenhuizen PT, Schwarzmann G, Möbius W, Hoernschemeyer J, Slot JW, Geuze HJ, Stoorvogel W (2003) Proteomic and biochemical analyses of human B cell-derived exosomes. Potential implications for their function and multivesicular body formation. J Biol Chem 278:10963–10972. https://doi.org/10.1074/jbc.M207550200
Yu T, MacPhail SH, Banáth JP, Klokov D, Olive PL (2006) Endogenous expression of phosphorylated histone H2AX in tumors in relation to DNA double-strand breaks and genomic instability. DNA Repair (Amst) 5:935–946. https://doi.org/10.1016/j.dnarep.2006.05.040
Zannikou M, Bellou S, Eliades P, Hatzioannou A, Mantzaris MD, Carayanniotis G, Avrameas S, Lymberi P (2016) DNA-histone complexes as ligands amplify cell penetration and nuclear targeting of anti-DNA antibodies via energy-independent mechanisms. Immunology 147:73–81. https://doi.org/10.1111/imm.12542
Zhang H, Freitas D, Kim HS, Fabijanic K, Li Z, Chen H, Mark MT, Molina H, Martin AB, Bojmar L, Fang J, Rampersaud S, Hoshino A, Matei I, Kenific CM, Nakajima M, Mutvei AP, Sansone P, Buehring W, Wang H, Jimenez JP, Cohen-Gould L, Paknejad N, Brendel M, Manova-Todorova K, Magalhães A, Ferreira JA, Osório H, Silva AM, Massey A, Cubillos-Ruiz JR, Galletti G, Giannakakou P, Cuervo AM, Blenis J, Schwartz R, Brady MS, Peinado H, Bromberg J, Matsui H, Reis CA, Lyden D (2018) Identification of distinct nanoparticles and subsets of extracellular vesicles by asymmetric flow field-flow fractionation. Nat Cell Biol 20:332–343. https://doi.org/10.1038/s41556-018-0040-4
Zhang Q, Higginbotham JN, Jeppesen DK et al (2019) Transfer of functional cargo in exomeres. Cell Rep 27:940–954.e6. https://doi.org/10.1016/j.celrep.2019.01.009
Zhao Y, Xiao A, diPierro CG, Carpenter JE, Abdel-Fattah R, Redpath GT, Lopes MB, Hussaini IM (2010) An extensive invasive intracranial human glioblastoma xenograft model. Am J Pathol 176:3032–3049. https://doi.org/10.2353/ajpath.2010.090571
Ziegler YS, Moresco JJ, Yates JR et al (2016) Integration of breast cancer secretomes with clinical data elucidates potential serum markers for disease detection, diagnosis, and prognosis. PLoS One 11:e0158296. https://doi.org/10.1371/journal.pone.0158296
Zijlstra A, Di Vizio D (2018) Size matters in nanoscale communication. Nat Cell Biol 20:228–230. https://doi.org/10.1038/s41556-018-0049-8
Zou H, Wen C, Peng Z, Shao YΥ, Hu L, Li S, Li C, Zhou HH (2017) P4HB and PDIA3 are associated with tumor progression and therapeutic outcome of diffuse gliomas. Oncol Rep 39:501–510. https://doi.org/10.3892/or.2017.6134
Funding
This study was financially supported by a grant from the Natural Sciences and Engineering Research Council of Canada (NSERC).
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Griffiths, S.G., Ezrin, A., Jackson, E. et al. A robust strategy for proteomic identification of biomarkers of invasive phenotype complexed with extracellular heat shock proteins. Cell Stress and Chaperones 24, 1197–1209 (2019). https://doi.org/10.1007/s12192-019-01041-8
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12192-019-01041-8