Isoelectric trapping and discrimination of histones from plasma in a microfluidic device using dehydrated isoelectric gate.

Agarose gate Fluorescence detection Histones Isoelectric trapping Microfluidics Sepsis Xurography

Journal

Mikrochimica acta
ISSN: 1436-5073
Titre abrégé: Mikrochim Acta
Pays: Austria
ID NLM: 7808782

Informations de publication

Date de publication:
13 Feb 2024
Historique:
received: 20 09 2023
accepted: 19 01 2024
medline: 14 2 2024
pubmed: 14 2 2024
entrez: 13 2 2024
Statut: epublish

Résumé

Histones are basic proteins with an isoelectric point around 11. It has been shown that the level of plasma circulating histones increases significantly during sepsis, and circulating free histones are associated with sepsis severity and mortality. It was found that the median plasma total free histone concentration of sepsis ICU non-survivors is higher compared to survivors. Therefore, histone concentration can serve as a prognostic indicator and there is a need for a simple, low-cost, and rapid method for measuring histone levels. In this work, we have developed a microfluidic device containing an isoelectric membrane made of dehydrated agarose gel of a specific pH embedded in a porous membrane for isoelectric trapping of histones rapidly. Although isoelectric gates have been used for trapping proteins before, they have to be introduced at the time of the experiment. Here, we show that isoelectric gates formed by gels loaded in a scaffold can be integrated directly into the fabrication process flow, dehydrated for storage, and rehydrated during the experiment and still function effectively to achieve isoelectric trapping. A low-cost and rapid microfabrication technique, xurography, was used for agarose integration and device fabrication. The integrated device was tested with samples containing buffered histone, histone in the presence of high-concentration bovine serum albumin (BSA), and histone spiked in blood plasma. The results show that the device can be used to distinguish between survivors and non-survivors of sepsis in less than 10 min, making it suitable as a point-of-care device for sepsis prognosis.

Identifiants

pubmed: 38351209
doi: 10.1007/s00604-024-06223-5
pii: 10.1007/s00604-024-06223-5
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

131

Informations de copyright

© 2024. The Author(s), under exclusive licence to Springer-Verlag GmbH Austria, part of Springer Nature.

Références

Nofi CP, Wang P, Aziz M (2022) Chromatin-associated molecular patterns (CAMPs) in sepsis. Cell Death Dis 13(8):700
doi: 10.1038/s41419-022-05155-3 pubmed: 35961978 pmcid: 9372964
Wildhagen KC, Wiewel MA, Schultz MJ, Horn J, Schrijver R, Reutelingsperger CP, van der Poll T, Nicolaes GA (2015) Extracellular histone H3 levels are inversely correlated with antithrombin levels and platelet counts and are associated with mortality in sepsis patients. Thromb Res 136(3):542–547
doi: 10.1016/j.thromres.2015.06.035 pubmed: 26232351
Marsman G, Zeerleder S, Luken BM (2016) Extracellular histones, cell-free DNA, or nucleosomes: differences in immunostimulation. Cell Death Dis 7(12):e2518–e2518
doi: 10.1038/cddis.2016.410 pubmed: 27929534 pmcid: 5261016
Li Y, Wan D, Luo X, Song T, Wang Y, Yu Q, Jiang L, Liao R, Zhao W, Su B (2021) Circulating histones in sepsis: potential outcome predictors and therapeutic targets. Front Immunol 12:650184
doi: 10.3389/fimmu.2021.650184 pubmed: 33868288 pmcid: 8044749
Gargano AF, Shaw JB, Zhou M, Wilkins CS, Fillmore TL, Moore RJ, Somsen GW, Paša-Tolić L (2018) Increasing the separation capacity of intact histone proteoforms chromatography coupling online weak cation exchange-HILIC to reversed phase LC UVPD-HRMS. J Proteome Res 17(11):3791–3800
doi: 10.1021/acs.jproteome.8b00458 pubmed: 30226781 pmcid: 6220366
Xu Z, Huang Y, Mao P, Zhang J, Li Y (2015) Sepsis and ARDS: the dark side of histones. Mediat Inflamm 2015:205054
Ito T, Nakahara M, Masuda Y, Ono S, Yamada S, Ishikura H, Imaizumi H, Kamikokuryo C, Kakihana Y, Maruyama I (2018) Circulating histone H3 levels are increased in septic mice in a neutrophil-dependent manner: preclinical evaluation of a novel sandwich ELISA for histone H3. J Intensive Care 6:1–6
doi: 10.1186/s40560-018-0348-y
Xu J, Zhang X, Pelayo R, Monestier M, Ammollo CT, Semeraro F, Taylor FB, Esmon NL, Lupu F, Esmon CT (2009) Extracellular histones are major mediators of death in sepsis. Nat Med 15(11):1318–1321
doi: 10.1038/nm.2053 pubmed: 19855397 pmcid: 2783754
Han Z, Yuan Z, Shu L, Li T, Yang F, Chen L (2023) Extracellular histone H3 facilitates ferroptosis in sepsis through ROS/JNK pathway. Immun, Inflamm Dis 11(1):e754
doi: 10.1002/iid3.754 pubmed: 36705411
Singer M, Deutschman CS, Seymour CW, Shankar-Hari M, Annane D, Bauer M, Bellomo R, Bernard GR, Chiche J-D, Coopersmith CM (2016) The third international consensus definitions for sepsis and septic shock (Sepsis-3). JAMA 315(8):801–810
doi: 10.1001/jama.2016.0287 pubmed: 26903338 pmcid: 4968574
Purcarea A, Sovaila S (2020) Sepsis, a 2020 review for the internist. Rom J Intern Med 58(3):129–137
pubmed: 32396142
Kumar A, Roberts D, Wood KE, Light B, Parrillo JE, Sharma S, Suppes R, Feinstein D, Zanotti S, Taiberg L (2006) Duration of hypotension before initiation of effective antimicrobial therapy is the critical determinant of survival in human septic shock. Crit Care Med 34(6):1589–1596
doi: 10.1097/01.CCM.0000217961.75225.E9 pubmed: 16625125
Cheng Z, Abrams ST, Alhamdi Y, Toh J, Yu W, Wang G, Toh C-H (2019) Circulating histones are major mediators of multiple organ dysfunction syndrome in acute critical illnesses. Crit Care Med 47(8):e677–e684
doi: 10.1097/CCM.0000000000003839 pubmed: 31162199
Eichhorn T, Linsberger I, Lauková L, Tripisciano C, Fendl B, Weiss R, König F, Valicek G, Miestinger G, Hörmann C (2021) Analysis of inflammatory mediator profiles in sepsis patients reveals that extracellular histones are strongly elevated in nonsurvivors. Mediat Inflamm 2021:8395048
Ekaney ML, Otto GP, Sossdorf M, Sponholz C, Boehringer M, Loesche W, Rittirsch D, Wilharm A, Kurzai O, Bauer M (2014) Impact of plasma histones in human sepsis and their contribution to cellular injury and inflammation. Crit Care 18(5):1–9
doi: 10.1186/s13054-014-0543-8
García-Giménez J, Romá-Mateo C, Carbonell N, Palacios L, Peiró-Chova L, García-López E, García-Simón M, Lahuerta R, Gimenez-Garzó C, Berenguer-Pascual E (2017) A new mass spectrometry-based method for the quantification of histones in plasma from septic shock patients. Sci Rep 7(1):1–10
doi: 10.1038/s41598-017-10830-z
Lu N-F, Jiang L, Zhu B, Yang D-G, Zheng R-Q, Shao J, Xi X-M (2020) Elevated plasma histone H4 level predicts increased risk of mortality in patients with sepsis. Ann Palliat Med 9:1084–1091
doi: 10.21037/apm-20-1011 pubmed: 32434363
Yokoyama Y, Ito T, Yasuda T, Furubeppu H, Kamikokuryo C, Yamada S, Maruyama I, Kakihana Y (2019) Circulating histone H3 levels in septic patients are associated with coagulopathy, multiple organ failure, and death: a single-center observational study. Thromb J 17(1):1–7
doi: 10.1186/s12959-018-0190-4 pubmed: 30651722 pmcid: 6330748
Zhan X, Liu D, Dong Y, Gao Y, Xu X, Xie T, Zhou H, Wang G, Zhang H, Wu P (2022) Early changes and predictive value of serum histone H3 concentration in urosepsis: a prospective observational study. Adv Ther 39(3):1310–1323
doi: 10.1007/s12325-021-02026-9 pubmed: 35066799 pmcid: 8918176
Abrams ST, Zhang N, Manson J, Liu T, Dart C, Baluwa F, Wang SS, Brohi K, Kipar A, Yu W (2013) Circulating histones are mediators of trauma-associated lung injury. Am J Respir Crit Care Med 187(2):160–169
doi: 10.1164/rccm.201206-1037OC pubmed: 23220920 pmcid: 3570656
Alhamdi Y, Abrams ST, Cheng Z, Jing S, Su D, Liu Z, Lane S, Welters I, Wang G, Toh C-H (2015) Circulating histones are major mediators of cardiac injury in patients with sepsis. Crit Care Med 43(10):2094–2103
doi: 10.1097/CCM.0000000000001162 pubmed: 26121070
Mai J, Sommer GJ, Hatch AV (2012) Microfluidic digital isoelectric fractionation for rapid multidimensional glycoprotein analysis. Anal Chem 84(8):3538–3545
doi: 10.1021/ac203076p pubmed: 22409593
Pergande MR, Cologna SM (2017) Isoelectric point separations of peptides and proteins. Proteomes 5(1):4
doi: 10.3390/proteomes5010004 pubmed: 28248255 pmcid: 5372225
Sommer GJ, Mai J, Singh AK, Hatch AV (2011) Microscale isoelectric fractionation using photopolymerized membranes. Anal Chem 83(8):3120–3125
doi: 10.1021/ac200073p pubmed: 21417312
Damodara S, Dwivedi DJ, Liaw PC, Fox-Robichaud AE, Selvaganapathy PR, Canadian Critical Care Translational Biology Group (2021) Single step separation and concentration of biomarker proteins using agarose based miniaturized isoelectric gates for point of care diagnostics. Sens Actuators B: Chemical 330:129265
doi: 10.1016/j.snb.2020.129265
Damodara S, Arora J, Dwivedi DJ, Liaw PC, Fox-Robichaud AE, Selvaganapathy PR, Canadian Critical Care Translational Biology Group (2022) Microfluidic device for single step measurement of protein C in plasma samples for sepsis prognosis. Lab on a Chip 22(13):2566–2577
doi: 10.1039/D1LC01084K pubmed: 35678179
Shahriari S, Selvaganapathy PR (2022) Integration of hydrogels into microfluidic devices with porous membranes as scaffolds enables their drying and reconstitution. Biomicrofluidics 16(5):054108
doi: 10.1063/5.0100589 pubmed: 36313189 pmcid: 9616609
Damodara S, Shahriari S, Wu W-I, Rezai P, Hsu H-H, Selvaganapathy R (2021) Materials and methods for microfabrication of microfluidic devices. In: Microfluidic devices for biomedical applications. Woodhead Publishing, Elsevier, pp 1–78 
Shahriari S, Patel V, Selvaganapathy PR (2023) Xurography as a tool for the fabrication of microfluidic devices. J Micromech Microeng 33:083002
Paul J, Veenstra TD (2022) Separation of serum and plasma proteins for in-depth proteomic analysis. Separations 9(4):89
doi: 10.3390/separations9040089
De M, Rana S, Akpinar H, Miranda OR, Arvizo RR, Bunz UH, Rotello VM (2009) Sensing of proteins in human serum using conjugates of nanoparticles and green fluorescent protein. Nat Chem 1(6):461–465
doi: 10.1038/nchem.334 pubmed: 20161380 pmcid: 2782604
Monteiro RC, Halbwachs-Mecarelli L, Roque-Barreira MC, Noel L-H, Berger J, Lesavre P (1985) Charge and size of mesangial IgA in IgA nephropathy. Kidney Int 28(4):666–671
doi: 10.1038/ki.1985.181 pubmed: 3910914
Barrett AJ, Brown MA, Sayers CA (1979) The electrophoretically ‘slow’and ‘fast’forms of the α2-macroglobulin molecule. Biochem J 181(2):401–418
doi: 10.1042/bj1810401 pubmed: 91367 pmcid: 1161172
Prin C, Bene MC, Gobert B, Montagne P, Faure GC (1995) Isoelectric restriction of human immunoglobulin isotypes. Biochim Biophys Acta (BBA)-General Subj 1243(2):287–289
doi: 10.1016/0304-4165(94)00187-3
Adler A, Manivel VA, Fromell K, Teramura Y, Ekdahl KN, Nilsson B (2022) A robust method to store complement C3 with superior ability to maintain the native structure and function of the protein. Front Immunol 13:891994
doi: 10.3389/fimmu.2022.891994 pubmed: 35592325 pmcid: 9110808
Ayyub A, Saleem M, Musharraf SG, Naz M, Tariq A, Hashmi N (2015) Mass spectrometric identification, characterization and validation of the haptoglobin β-chain protein as a lung cancer serum biomarker. Mol Med Rep 12(3):3755–3762
doi: 10.3892/mmr.2015.3822 pubmed: 26005016
Leeman M, Choi J, Hansson S, Storm MU, Nilsson L (2018) Proteins and antibodies in serum, plasma, and whole blood—size characterization using asymmetrical flow field-flow fractionation (AF4). Anal Bioanal Chem 410:4867–4873
doi: 10.1007/s00216-018-1127-2 pubmed: 29808297 pmcid: 6061777
Fullarton J, Kenny A (1970) A rapid system for preparative electrophoresis depending on isoelectric buffers of low conductivity. Biochemical Journal 116(1):147
doi: 10.1042/bj1160147 pubmed: 5460789 pmcid: 1185333
Dötsch V, Withers RS (2005) Low-conductivity buffers for magnetic resonance measurements. U.S. Patent 6,958,244
Wiig H, Kolmannskog O, Tenstad O, Bert JL (2003) Effect of charge on interstitial distribution of albumin in rat dermis in vitro. J Physiol 550(2):505–514
doi: 10.1113/jphysiol.2003.042713 pubmed: 12766239 pmcid: 2343033

Auteurs

Shadi Shahriari (S)

Department of Mechanical Engineering, McMaster University, Hamilton, ON, Canada.

Sreekant Damodara (S)

Department of Mechanical Engineering, McMaster University, Hamilton, ON, Canada.

P Ravi Selvaganapathy (PR)

Department of Mechanical Engineering, McMaster University, Hamilton, ON, Canada. selvaga@mcmaster.ca.
School of Biomedical Engineering, McMaster University, Hamilton, ON, Canada. selvaga@mcmaster.ca.

Classifications MeSH