Imaging oxygen in neural cell and tissue models by means of anionic cell-permeable phosphorescent nanoparticles

Cellular and Molecular Life Sciences

Volumn 72, Issue 2, 2015, Pages 367-381

  Dmitriev, Ruslan I ^a   Borisov, Sergey M ^b   Kondrashina, Alina V ^a   Pakan, Janelle M P ^a   Anilkumar, Ujval ^c   Prehn, Jochen H M ^c   Zhdanov, Alexander V ^a   McDermott, Kieran W ^a   Klimant, Ingo ^b   Papkovsky, Dmitri B ^a  

^a UNIVERSITY COLLEGE CORK   (Ireland)

^b GRAZ UNIVERSITY OF TECHNOLOGY   (Austria)

^c ROYAL COLLEGE OF SURGEONS IN IRELAND   (Ireland)

Author keywords

Biomaterials; Cell and tissue oxygen; Intracellular oxygen probe; Multiplexed detection; Nanosensors; Phosphorescence quenching microscopy; PLIM

Indexed keywords

MOLECULAR PROBE; NANOPARTICLE; OXYGEN;

AGE; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; LUMINESCENCE; METABOLISM; MOLECULAR IMAGING; MOLECULAR PROBE; NERVE CELL; PROCEDURES; RAT;

AGE FACTORS; ANIMALS; LUMINESCENT MEASUREMENTS; MOLECULAR IMAGING; MOLECULAR PROBES; MOLECULAR STRUCTURE; NANOPARTICLES; NEURONS; OXYGEN; RATS;

EID: 84930205944     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-014-1673-5     Document Type: Article

References (75)

1. Kobayashi H, Ogawa M, Alford R, Choyke PL, Urano Y (2009) New strategies for fluorescent probe design in medical diagnostic imaging. Chem Rev 110(5):2620-2640
2. Schäferling M (2012) The art of fluorescence imaging with chemical sensors. Angew Chem Int Ed 51(15):3532-3554. doi: 10.1002/anie.201105459
3. Algar WR, Prasuhn DE, Stewart MH, Jennings TL, Blanco-Canosa JB, Dawson PE, Medintz IL (2011) The controlled display of biomolecules on nanoparticles: a challenge suited to bioorthogonal chemistry. Bioconjug Chem 22(5):825-858
4. Canton I, Battaglia G (2012) Endocytosis at the nanoscale. Chem Soc Rev 41(7):2718-2739
5. Soenen SJ, Himmelreich U, Nuytten N, Pisanic TR, Ferrari A, De Cuyper M (2010) Intracellular nanoparticle coating stability determines nanoparticle diagnostics efficacy and cell functionality. Small 6(19):2136-2145
6. Karamchand L, Kim G, Wang S, Hah HJ, Ray A, Jiddou R, Koo Lee Y-E, Philbert MA, Kopelman R (2013) Modulation of hydrogel nanoparticle intracellular trafficking by multivalent surface engineering with tumor targeting peptide. Nanoscale 5(21):10327-10344. doi: 10.1039/c3nr00908d
7. Koo Lee Y-E, Ulbrich EE, Kim G, Hah H, Strollo C, Fan W, Gurjar R, Koo S, Kopelman R (2010) Near infrared luminescent oxygen nanosensors with nanoparticle matrix tailored sensitivity. Anal Chem 82(20):8446-8455. doi: 10.1021/ac1015358
8. Napp J, Behnke T, Fischer L, Würth C, Wottawa M, Katschinski DM, Alves F, Resch-Genger U, Schäferling M (2011) Targeted luminescent near-infrared polymer-nanoprobes for in vivo imaging of tumor hypoxia. Anal Chem 83(23):9039-9046. doi: 10.1021/ac201870b
9. Xiang H, Cheng J, Ma X, Zhou X, Chruma JJ (2013) Near-infrared phosphorescence: materials and applications. Chem Soc Rev. doi: 10.1039/c3cs60029g
10. Dmitriev RI, Papkovsky DB (2012) Optical probes and techniques for O2 measurement in live cells and tissue. Cell Mol Life Sci 69(12):2025-2039
11. Quaranta M, Borisov SM, Klimant I (2012) Indicators for optical oxygen sensors. Bioanal Rev 4(2-4):115-157
12. Ruggi A, van Leeuwen FW, Velders AH (2011) Interaction of dioxygen with the electronic excited state of Ir(III) and Ru (II) complexes: principles and biomedical applications. Coord Chem Rev 255(21):2542-2554
13. Lee Y-EK, Kopelman R, Smith R (2009) Nanoparticle PEBBLE sensors in live cells and in vivo. Annu Rev Anal Chem (Palo Alto, Calif) 2:57
14. Devor A, Sakadžić S, Yaseen MA, Roussakis E, Tian P, Slovin H, Vanzetta I, Teng I, Saisan PA, Sinks LE (2014) Functional imaging of cerebral oxygenation with intrinsic optical contrast and phosphorescent probes. Optical imaging of neocortical dynamics. Springer, Berlin, pp 225-253
15. Papkovsky DB, Dmitriev RI (2013) Biological detection by optical oxygen sensing. Chem Soc Rev 42(22):8700-8732
16. Tsytsarev V, Arakawa H, Borisov S, Pumbo E, Erzurumlu RS, Papkovsky DB (2013) In vivo imaging of brain metabolism activity using a phosphorescent oxygen-sensitive probe. J Neurosci Methods 216(2):146-151
17. Dmitriev RI, Zhdanov AV, Nolan YM, Papkovsky DB (2013) Imaging of neurosphere oxygenation with phosphorescent probes. Biomaterials 34(37):9307-9317
18. Lambrechts D, Roeffaers M, Kerckhofs G, Roberts SJ, Hofkens J, Van de Putte T, Van Oosterwyck H, Schrooten J (2013) Fluorescent oxygen sensitive microbead incorporation for measuring oxygen tension in cell aggregates. Biomaterials 34(4):922-929
19. Dmitriev RI, Kondrashina AV, Koren K, Klimant I, Zhdanov AV, Pakan JMP, McDermott KW, Papkovsky DB (2014) Small molecule phosphorescent probes for O2 imaging in 3D tissue models. Biomater Sci 2:853-866. doi: 10.1039/c3bm60272a
20. Dmitriev RI, Zhdanov AV, Jasionek G, Papkovsky DB (2012) Assessment of cellular oxygen gradients with a panel of phosphorescent oxygen-sensitive probes. Anal Chem 84(6):2930-2938
21. Zhdanov AV, Dmitriev RI, Golubeva AV, Gavrilova SA, Papkovsky DB (1830) Chronic hypoxia leads to a glycolytic phenotype and suppressed HIF-2 signaling in PC12 cells. Biochim Biophys Acta Gen Subj 6:3553-3569
22. Zhdanov AV, Waters AH, Golubeva AV, Dmitriev RI, Papkovsky DB (1837) Availability of the key metabolic substrates dictates the respiratory response of cancer cells to the mitochondrial uncoupling. Biochim Biophys Acta Bioenerg 1:51-62
23. Apreleva SV, Wilson DF, Vinogradov SA (2006) Tomographic imaging of oxygen by phosphorescence lifetime. Appl Opt 45(33):8547-8559
24. Zhdanov AV, Ogurtsov VI, Taylor CT, Papkovsky DB (2010) Monitoring of cell oxygenation and responses to metabolic stimulation by intracellular oxygen sensing technique. Integr Biol 2(9):443-451
25. Takahashi E, Asano K (2002) Mitochondrial respiratory control can compensate for intracellular O2 gradients in cardiomyocytes at low Po 2. Am J Physiol Heart Circ Physiol 283(3):H871-H878
26. Finikova OS, Lebedev AY, Aprelev A, Troxler T, Gao F, Garnacho C, Muro S, Hochstrasser RM, Vinogradov SA (2008) Oxygen microscopy by two-photon-excited phosphorescence. ChemPhysChem 9(12):1673-1679
27. Mik EG, Stap J, Sinaasappel M, Beek JF, Aten JA, van Leeuwen TG, Ince C (2006) Mitochondrial PO2 measured by delayed fluorescence of endogenous protoporphyrin IX. Nat Methods 3(11):939-945
28. Clanton T, Hogan M, Gladden L (2013) Regulation of cellular gas exchange, oxygen sensing, and metabolic control. Compr Physiol. doi: 10.1002/cphy.c120030
29. Erecińska M, Silver IA (2001) Tissue oxygen tension and brain sensitivity to hypoxia. Respir Physiol 128(3):263-276
30. Mohyeldin A, Garzón-Muvdi T, Quiñones-Hinojosa A (2010) Oxygen in stem cell biology: a critical component of the stem cell niche. Cell Stem Cell 7(2):150-161
31. Toussaint O, Weemaels G, Debacq-Chainiaux F, Scharffetter-Kochanek K, Wlaschek M (2011) Artefactual effects of oxygen on cell culture models of cellular senescence and stem cell biology. J Cell Physiol 226(2):315-321
32. Semenza GL (2009) Regulation of oxygen homeostasis by hypoxia-inducible factor 1. Physiology 24(2):97-106
33. McHugh SB, Fillenz M, Lowry JP, Rawlins JNP, Bannerman DM (2011) Brain tissue oxygen amperometry in behaving rats demonstrates functional dissociation of dorsal and ventral hippocampus during spatial processing and anxiety. Eur J Neurosci 33(2):322-337
34. Choi SW, Gerencser AA, Ng R, Flynn JM, Melov S, Danielson SR, Gibson BW, Nicholls DG, Bredesen DE, Brand MD (2012) No consistent bioenergetic defects in presynaptic nerve terminals isolated from mouse models of Alzheimer's disease. J Neurosci 32(47):16775-16784
35. Nicholls DG, Johnson-Cadwell L, Vesce S, Jekabsons M, Yadava N (2007) Bioenergetics of mitochondria in cultured neurons and their role in glutamate excitotoxicity. J Neurosci Res 85(15):3206-3212. doi: 10.1002/jnr.21290
36. Lancaster MA, Renner M, Martin C-A, Wenzel D, Bicknell LS, Hurles ME, Homfray T, Penninger JM, Jackson AP, Knoblich JA (2013) Cerebral organoids model human brain development and microcephaly. Nature 501:373-379. doi: 10.1038/nature12517
37. Noraberg J, Kristensen BW, Zimmer J (1999) Markers for neuronal degeneration in organotypic slice cultures. Brain Res Protoc 3(3):278-290. doi: 10.1016/S1385-299X(98)00050-6
38. Zimmer J, Kristensen BW, Jakobsen B, Noraberg J (2000) Excitatory amino acid neurotoxicity and modulation of glutamate receptor expression in organotypic brain slice cultures. Amino Acids 19(1):7-21
39. Kazmi S, Salvaggio AJ, Estrada AD, Hemati MA, Shaydyuk NK, Roussakis E, Jones TA, Vinogradov SA, Dunn AK (2013) Three-dimensional mapping of oxygen tension in cortical arterioles before and after occlusion. Biomed Optics Express 4(7):1061-1073
40. Lecoq J, Parpaleix A, Roussakis E, Ducros M, Houssen YG, Vinogradov SA, Charpak S (2011) Simultaneous two-photon imaging of oxygen and blood flow in deep cerebral vessels. Nat Med 17(7):893-898
41. Wolfbeis OS (2013) Editorial: probes, sensors, and labels: Why is real progress slow? Angew Chem Int Ed 52(38):9864-9865. doi: 10.1002/anie.201305915
42. Kondrashina AV, Dmitriev RI, Borisov SM, Klimant I, O'Brien I, Nolan YM, Zhdanov AV, Papkovsky DB (2012) A phosphorescent nanoparticle-based probe for sensing and imaging of (Intra) cellular oxygen in multiple detection modalities. Adv Funct Mater 22(23):4931-4939. doi: 10.1002/adfm.201201387
43. Liu H, Yang H, Hao X, Xu H, Lv Y, Xiao D, Wang H, Tian Z (2013) Development of polymeric nanoprobes with improved lifetime dynamic range and stability for intracellular oxygen sensing. Small 9(15):2639-2648
44. X-d Wang, Gorris HH, Stolwijk JA, Meier RJ, Groegel DB, Wegener J, Wolfbeis OS (2011) Self-referenced RGB colour imaging of intracellular oxygen. Chem Sci 2(5):901-906
45. X-d Wang, Stolwijk JA, Lang T, Sperber M, Meier RJ, Wegener J, Wolfbeis OS (2012) Ultra-small, highly stable, and sensitive dual nanosensors for imaging intracellular oxygen and pH in cytosol. J Am Chem Soc 134(41):17011-17014
46. Wu C, Bull B, Christensen K, McNeill J (2009) Ratiometric single-nanoparticle oxygen sensors for biological imaging. Angew Chem Int Ed 48(15):2741-2745
47. Yim H, S-j Park, Bae YH, Na K (2013) Biodegradable cationic nanoparticles loaded with an anticancer drug for deep penetration of heterogeneous tumours. Biomaterials 34(31):7674-7682
48. Owens Iii DE, Peppas NA (2006) Opsonization, biodistribution, and pharmacokinetics of polymeric nanoparticles. Int J Pharm 307(1):93-102. doi: 10.1016/j.ijpharm.2005.10.010
49. Ingram J, Zhang C, Cressman JR, Hazra A, WEI Y, Koo Y-E, Ziburkus J, Kopelman R, Xu J, Schiff SJ (2014) Oxygen and seizure dynamics: I. Experiments. J Neurophysiol 00540:02013
50. Ingram JM, Zhang C, Xu J, Schiff SJ (2013) FRET excited ratiometric oxygen sensing in living tissue. J Neurosci Methods 214(1):45-51. doi: 10.1016/j.jneumeth.2013.01.002
51. Koren K, Dmitriev RI, Borisov SM, Papkovsky DB, Klimant I (2012) Complexes of IrIII-Octaethylporphyrin with Peptides as Probes for Sensing Cellular O2. Chembiochem 13(8):1184-1190. doi: 10.1002/cbic.201200083
52. Borisov SM, Mayr T, Mistlberger G, Waich K, Koren K, Chojnacki P, Klimant I (2009) Precipitation as a simple and versatile method for preparation of optical nanochemosensors. Talanta 79(5):1322-1330
53. Albanese A, Tang PS, Chan WC (2012) The effect of nanoparticle size, shape, and surface chemistry on biological systems. Annu Rev Biomed Eng 14:1-16
54. Yang W-H, Smolen VF, Peppas NA (1981) Oxygen permeability coefficients of polymers for hard and soft contact lens applications. J Membr Sci 9(1):53-67
55. Fercher A, Borisov SM, Zhdanov AV, Klimant I, Papkovsky DB (2011) Intracellular O2 sensing probe based on cell-penetrating phosphorescent nanoparticles. ACS Nano 5(7):5499-5508
56. Mendes AN, Hubber I, Siqueira M, Barbosa GM, de Lima Moreira D, Holandino C, Pinto JC, Nele M (2012) Preparation and Cytotoxicity of Poly (Methyl Methacrylate) Nanoparticles for Drug Encapsulation. In: Macromolecular Symposia, Wiley Online Library, pp 34-40
57. Araujo L, Sheppard M, Löbenberg R, Kreuter J (1999) Uptake of PMMA nanoparticles from the gastrointestinal tract after oral administration to rats: modification of the body distribution after suspension in surfactant solutions and in oil vehicles. Int J Pharm 176(2):209-224
58. Ivanov AI (2008) Pharmacological inhibition of endocytic pathways: is it specific enough to be useful? In: Exocytosis and Endocytosis. Springer, pp 15-33
59. Carraway E, Demas J, DeGraff B, Bacon J (1991) Photophysics and photochemistry of oxygen sensors based on luminescent transition-metal complexes. Anal Chem 63(4):337-342
60. DeGraff B, Demas J (2005) Luminescence-based oxygen sensors. Reviews in Fluorescence 2005:125-151
61. Foster KA, Galeffi F, Gerich FJ, Turner DA, Müller M (2006) Optical and pharmacological tools to investigate the role of mitochondria during oxidative stress and neurodegeneration. Prog Neurobiol 79(3):136-171
62. Pakan JM, McDermott KW (2014) A method to investigate radial glia cell behavior using two-photon time-lapse microscopy in an ex vivo model of spinal cord development. Front Neuroanat 8:22. doi: 10.3389/fnana.2014.00022
63. Schmid RS, Yokota Y, Anton E (2006) Generation and characterization of brain lipid-binding protein promoter-based transgenic mouse models for the study of radial glia. Glia 53(4):345-351
64. Becker W (2012) Fluorescence lifetime imaging - techniques and applications. J Microsc 247(2):119-136. doi: 10.1111/j.1365-2818.2012.03618.x
65. Ingaramo M, York AG, Wawrzusin P, Milberg O, Hong A, Weigert R, Shroff H, Patterson GH (2014) Two-photon excitation improves multifocal structured illumination microscopy in thick scattering tissue. Proc Natl Acad Sci 111(14):5254-5259
66. Pampaloni F, Ansari N, Stelzer EH (2013) High-resolution deep imaging of live cellular spheroids with light-sheet-based fluorescence microscopy. Cell Tissue Res 352:161-177
67. Golub AS, Pittman RN (2008) PO2 measurements in the microcirculation using phosphorescence quenching microscopy at high magnification. Am J Physiol Heart Circ Physiol 63(6):H2905
68. Devor A, Sakadzic S, Srinivasan VJ, Yaseen MA, Nizar K, Saisan PA, Tian P, Dale AM, Vinogradov SA, Franceschini MA, Boas DA (2012) Frontiers in optical imaging of cerebral blood flow and metabolism. J Cereb Blood Flow Metab 32(7):1259-1276
69. Spencer JA, Ferraro F, Roussakis E, Klein A, Wu J, Runnels JM, Zaher W, Mortensen LJ, Alt C, Turcotte R, Yusuf R, Cote D, Vinogradov SA, Scadden DT, Lin CP (2014) Direct measurement of local oxygen concentration in the bone marrow of live animals. Nature advance online publication. doi: 10.1038/nature13034
70. Verma A, Stellacci F (2010) Effect of surface properties on nanoparticle-cell interactions. Small 6(1):12-21. doi: 10.1002/smll.200901158
71. Nichols AJ, Roussakis E, Klein OJ, Evans CL (2014) Click-Assembled, Oxygen-Sensing Nanoconjugates for Depth-Resolved, Near-Infrared Imaging in a 3 D Cancer Model. Angew Chem Int Ed n/a-n/a. doi: 10.1002/anie.201311303
72. Dmitriev RI, Ropiak HM, Ponomarev GV, Yashunsky DV, Papkovsky DB (2011) Cell-penetrating conjugates of coproporphyrins with oligoarginine peptides: rational design and application for sensing intracellular O2. Bioconjugate Chem 22(12):2507-2518
73. Anilkumar U, Weisová P, Düssmann H, Concannon CG, König H-G, Prehn JHM (2013) AMP-activated protein kinase (AMPK)-induced preconditioning in primary cortical neurons involves activation of MCL-1. J Neurochem 124(5):721-734. doi: 10.1111/jnc.12108
74. Stoppini L, Buchs P-A, Muller D (1991) A simple method for organotypic cultures of nervous tissue. J Neurosci Methods 37(2):173-182
75. Murphy RC, Messer A (2001) Gene transfer methods for CNS organotypic cultures: a comparison of three nonviral methods. Mol Ther 3(1):113-121