Identification, localization, and quantification of neuronal cell membrane receptors with plasmonic probes: Role of protein kinase D1 in their distribution

ACS Nano

Volumn 8, Issue 9, 2014, Pages 8942-8958

  Fraire, Juan C ^a   Masseroni, M Lujan ^b   Jausoro, Ignacio ^b   Perassi, Eduardo M ^a   Diaz Anel, Alberto M ^b   Coronado, Eduardo A ^a  

^a Departamento de Fisicoquímia   (Argentina)

^b UNIVERSIDAD NACIONAL DE CÓRDOBA   (Argentina)

Author keywords

Bioconjugation; Immunolabels; Nanoparticles; Neurons; Neurotransmitter receptors; PKD1; Plasmonics; Sensing; Sorting

Indexed keywords

BIOLOGICAL MEMBRANES; CELL MEMBRANES; CELLS; ENZYMES; GOLD; MAPPING; MEMBRANES; MOLECULAR BIOLOGY; NANOPARTICLES; NEURONS; PLASMONS; PROBES; PROTEINS; SCANNING ELECTRON MICROSCOPY; SORTING; SPATIAL DISTRIBUTION;

BIO-CONJUGATION; IMMUNOLABELS; NEUROTRANSMITTER RECEPTORS; PKD1; PLASMONICS; SENSING;

CYTOLOGY;

GOLD; METABOTROPIC GLUTAMATE RECEPTOR TYPE 1; METABOTROPIC RECEPTOR; METAL NANOPARTICLE; MOLECULAR PROBE; PROTEIN KINASE C; PROTEIN KINASE D;

ANIMAL; CELL MEMBRANE; CHEMISTRY; CYTOLOGY; FLUORESCENCE IMAGING; GENE EXPRESSION REGULATION; METABOLISM; MOLECULAR PROBE; NERVE CELL; NERVE FIBER; PROTEIN TRANSPORT; RAT;

ANIMALS; AXONS; CELL MEMBRANE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GOLD; METAL NANOPARTICLES; MOLECULAR PROBES; NEURONS; OPTICAL IMAGING; PROTEIN KINASE C; PROTEIN TRANSPORT; RATS; RECEPTORS, METABOTROPIC GLUTAMATE;

EID: 84927609991     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/nn501575c     Document Type: Article

References (70)

1. Martin, F. L.; Kelly, J. G.; Llabjani, V.; Martin-Hirsch, P. L.; Patel, I. I.; Trevisan, J.; Fullwood, N. J.; Walsh, M. J. Distinguishing Cell Types or Populations Based on the Computational Analysis of their Infrared Spectra. Nat. Protoc. 2010, 5, 1748-1760.
2. Yi, C.; Liu, D.; Yang, M. Building Nanoscale Architectures by Directed Synthesis and Self-Assembly. Curr. Nanosci. 2009, 5, 75-87.
3. Fraire, J. C.; Pérez, L. A.; Coronado, E. A. Rational Design of Plasmonic Nanostructures for Biomolecular Detection: Interplay between Theory and Experiments. ACS Nano 2012, 6, 3441-3452.
4. Gregas, M. K.; Scaffidi, J. P.; Lauly, B.; Vo-Dinh, T. Surface-Enhanced Raman Scattering Detection and Tracking of Nanoprobes: Enhanced Uptake and Nuclear Targeting in Single Cells. Appl. Spectrosc. 2010, 8, 858-866.
5. Hodges, M. D.; Kelly, J. G.; Bentley, A. J.; Fogarty, S.; Patel, I. I.; Martin, F. L.; Fullwood, N. J. Combining Immunolabeling and Surface-Enhanced Raman Spectroscopy on Cell Membranes. ACS Nano 2011, 5, 9535-9541.
6. Wang, H. Y.; Rong, G. X.; Yan, B.; Yang, L. L.; Reinhard, B. M. Optical Sizing of Immunolabel Clusters through Multi-spectral Plasmon Coupling Microscopy. Nano Lett. 2011, 11, 498-504.
7. Wang, J.; Boriskina, S. V.; Wang, H.; Reinhard, B. M. Illuminating Epidermal Growth Factor Receptor Densities on Filopodia through Plasmon Coupling. ACS Nano 2011, 5, 6619-6628.
8. Rong, G. X.; Wang, H. Y.; Skewis, L. R.; Reinhard, B. M. Resolving Sub-Diffraction Limit Encounters in Nanoparti-cle Tracking Using Live Cell Plasmon Coupling Microscopy. Nano Lett. 2008, 8, 3386-3393.
9. Crow, M. J.; Grant, G.; Provenzale, J. M.; Wax, A. Molecular Imaging and Quantitative Measurement of Epidermal Growth Factor Receptor Expression in Live Cancer Cells Using Immunolabeled Gold Nanoparticles. Am. J. Roent-genol. 2009, 192, 1021-1028.
10. Aaron, J.; Travis, K.; Harrison, N.; Sokolov, K. Dynamic Imaging of Molecular Assemblies in Live Cells Based on Nanoparticle Plasmon Resonance Coupling. Nano Lett. 2009, 9, 3612-3618.
11. Austin, L. A.; Kang, B.; Yen, C. W.; El-Sayed, M. A. Plasmonic Imaging of Human Oral Cancer Cell Communities during Programmed Cell Death by Nuclear-Targeting Silver Nano-particles. J. Am. Chem. Soc. 2011, 133, 17594-17597.
12. Qian, W.; Huang, X. H.; Kang, B.; El-Sayed, M. A. Dark-Field Light Scattering Imaging of Living Cancer Cell Component from Birth through Division Using Bioconjugated Gold Nanoprobes. J. Biomed. Opt. 2010, 15, 046025.
13. Seekell, K.; Crow, M. J.; Marinakos, S.; Ostrander, J.; Chilkoti, A.; Wax, A. Hyperspectral Molecular Imaging of Multiple Receptors Using Immunolabeled Plasmonic Nanoparti-cles. J. Biomed. Opt. 2011, 16, 116003.
14. Crow, M. J.; Seekell, K.; Ostrander, J. H.; Wax, A. Monitoring of Receptor Dimerization Using Plasmonic Coupling of Gold Nanoparticles. ACS Nano 2011, 5, 8532-8540.
15. Kennedy, D. C.; Tay, L. L.; Lyn, R. K.; Rouleau, Y.; Hulse, J.; Pezacki, J. P. Nanoscale Aggregation of Cellular β2-Adrenergic Receptors Measured by Plasmonic Interactions of Function-alized Nanoparticles. ACS Nano 2009, 3, 2329-2339.
16. Wang, J.; Yu, X.; Boriskina, S. V.; Reinhard, B. M. Quantification of Differential ErbB1 and ErbB2 Cell Surface Expression and Spatial Nanoclustering through Plasmon Coupling. Nano Lett. 2011, 5, 6619-6628.
17. Hodges, M. D.; Kelly, J. G.; Bentley, A. J.; Fogarty, S.; Patel, I. I.; Martin, F. L.; Fullwood, N. J. Combining Immunolabeling and Surface-Enhanced Raman Spectroscopy on Cell Membranes. ACS Nano 2011, 5, 9535-9541.
18. Ahijado-Guzmán, R.; Gomez-Puertas, P.; Alvarez-Puebla, R. A.; Rivas, G.; Liz-Marzán, L. M. Surface-Enhanced Raman Scattering-Based Detection of the Interactions between the Essential Cell Division FtsZ Protein and Bacterial Membrane Elements. ACS Nano 2012, 6, 7514-7520.
19. Fullwood, N. J.; Davies, Y.; Nieduszynski, I. A.; Marcyniuk, B.; Ridgway, A. E.; Quantock, A. J. Cell Surface-Associated Keratan Sulphate on Normal and Migrating Corneal En-dothelium. Invest. Ophthalmol. Vis. Sci. 1996, 37, 1256-1270.
20. Herpers, B.; Xanthakis, D.; Rabouille, C. ISH-IEM: A Sensitive Method to Detect Endogenous mRNAs at the Ultrastruc-tural Level. Nat. Protoc. 2010, 5, 678-687.
21. Chen, L.; Wei, H.; Guo, Y.; Cui, Z.; Zhang, Z.; Zhang, X. E. sGold Nanoparticle Enhanced Immuno-PCR for Ultrasensitive Detection of Hantaan Virus Nucleocapsid Protein. J. Immunol. Methods 2009, 346, 64-70.
22. Potucková, L.; Franko, F.; Bambousková, M.; Dráber, P. Rapid and Sensitive Detection of Cytokines Using Func-tionalized Gold Nanoparticle-Based Immuno-PCR, Comparison with Immuno-PCR and ELISA. J. Immunol. Methods 2011, 371, 38-47.
23. Yang, S.; Raymond-Stintz, M. A.; Ying, W.; Zhang, J.; Lidke, D. S.; Steinberg, S. L.; Williams, L.; Oliver, J. M.; Wilson, B. S. Mapping ErbB Receptors on Breast Cancer Cell Membranes during Signal Transduction. J. Cell Sci. 2007, 120, 2763-2773.
24. Lessard, A.; Coleman, C. G.; Pickel, V. M. Chronic Intermittent Hypoxia Reduces Neurokinin-1 (NK1) Receptor Density in Small Dendrites of Non-catecholaminergic Neurons in Mouse Nucleus Tractus Solitarius. Exp. Neurol. 2010, 223, 634-644.
25. Stump, R. F.; Pfeiffer, J. R.; Seagrave, J.; Oliver, J. M. Mapping Gold-Labeled IgE Receptors on Mast Cells by Scanning Electron Microscopy: Receptor Distributions Revealed by Silver Enhancement, Backscattered Electron Imaging, and Digital Image Analysis. J. Histochem. Cytochem. 1988, 36, 493-503.
26. Crow, M. J.; Grant, G.; Provenzale, J. M.; Wax, A. Molecular Imaging and Quantitative Measurement of Epidermal Growth Factor Receptor Expression in Live Cancer Cells Using Immunolabeled Gold Nanoparticles. AJR Am. J. Roentgenol. 2009, 192, 1021-1028.
27. Kelly, K. L.; Coronado, E. A.; Zhao, L. L.; Schatz, G. C. The Optical Properties of Metal Nanoparticles: The Influence of Size, Shape, and Dielectric Environment. J. Phys. Chem. B 2003, 107, 668-677.
28. Perassi, E. M.; Hernandez-Garriddo, J. C.; Moreno, M. S.; Encina, E. R.; Coronado, E. A.; Midgley, P. A. Using Highly Accurate 3D Nanometrology to Model the Optical Properties of Highly Irregular Nanoparticles: A Powerful Tool for Rational Design of Plasmonic Devices. Nano Lett. 2010, 10, 2097-2104.
29. Kambhampati, P.; Child, C. M.; Foster, M. C.; Campion, A. On the Chemical Mechanism of Surface Enhanced Raman Scattering: Experiment and Theory. J. Chem. Phys. 1998, 108, 5013-5026.
30. Li, S.; Pedano, M. L.; Chang, S.-H.; Mirkin, C. A.; Schatz, G. C. Gap Structure Effects on Surface-Enhanced Raman Scattering Intensities for Gold Gapped Rods. Nano Lett. 2010, 10, 1722-1727.
31. Su, K. H.; Wei, Q. H.; Zhang, X.; Mock, J. J.; Smith, D. R.; Schultz, S. Interparticle Coupling Effects on Plasmon Resonances of Nanogold Particles. Nano Lett. 2003, 3, 1087-1090.
32. Jiang, J.; Bosnick, K.; Maillard, M.; Brus, L. Single Molecule Raman Spectroscopy at the Junctions of Large Ag Nano-crystals. J. Phys. Chem. B 2003, 107, 9964-9972.
33. Gunnarsson, L.; Bjerneld, E. J.; Xu, H.; Petronis, S.; Kasemo, B.; Kall, M. Interparticle Coupling Effects in Nanofabricated Substrates for Surface-Enhanced Raman Scattering. Appl. Phys. Lett. 2001, 78, 802-804.
34. Jain, P. K.; El-Sayed, M. A. Surface Plasmon Coupling and Its Universal Size Scaling in Metal Nanostructures of Complex Geometry: Elongated Particle Pairs and Nanosphere Trimers. J. Phys. Chem. C 2008, 112, 4954-4960.
35. Rechberger, W.; Hohenau, A.; Leitner, A.; Krenn, J. R.; Lamprecht, B.; Aussenegg, F. R. Optical Properties of Two Interacting Gold Nanoparticles. Opt. Commun. 2003, 220, 137-141.
36. Xu, H. X.; Aizpurua, J.; Kall, M.; Apell, P. Electromagnetic Contributions to Single-Molecule Sensitivity in Surface-Enhanced Raman Scattering. Phys. Rev. E 2000, 62, 4318-4324.
37. Prodan, E.; Radloff, C.; Halas, N. J.; Nordlander, P. A Hybridization Model for the Plasmon Response of Complex Nanostructures. Science 2003, 302, 419-422.
38. Halas, N. J.; Lal, S.; Chang, W. S.; Link, S.; Nordlander, P. Plasmons in Strongly Coupled Metallic Nanostructures. Chem. Rev. 2011, 111, 3913-3961.
39. Rozengurt, E. J.; Sinnett-Smith, J.; Van Lint, J.; Valverde, A. M. Protein Kinase D (PKD): A Novel Target for Dyacylglycerol and Phorbol Esters. Mutat. Res. 2005, 333, 153-160.
40. Díaz Añel, A. M.; Malhotra, V. PKCeta Is Required for Beta1gamma2/Beta3gamma2- and PKD-Mediated Transport to the Cell Surface and the Organization of the Golgi Apparatus. J. Cell Biol. 2005, 169, 83-91.
41. Rozengurt, E. Protein Kinase D Signaling: Multiple Biological Functions in Health and Disease. Physiology (Bethesda) 2011, 26, 23-33.
42. Díaz Añel, A. M. Phospholipase C Beta3 Is a Key Component in the Gbetagamma/PKCeta/PKD-Mediated Regulation of Trans-Golgi Network to Plasma Membrane Transport. Biochem. J. 2007, 406, 157-165.
43. Fu, Y.; Rubin, C. S. Protein Kinase D: Coupling Extracellular Stimuli to the Regulation of Cell Physiology. EMBO Rep. 2011, 12, 785-796.
44. Olayioye, M. A.; Barisic, S.; Hausser, A. Multi-Level Control of Actin Dynamics by Protein Kinase D. Cell Signal 2013, 25, 1739-1747.
45. Ellwanger, K.; Hausser, A. Physiological Functions of Protein Kinase D in Vivo. IUBMB Life 2013, 65, 98-107.
46. Bard, F.; Malhotra, V. The Formation of TGN-To-Plasma-Membrane Transport Carriers. Annu. Rev. Cell Dev. Biol. 2006, 22, 439-455.
47. Malhotra, V.; Campelo, F. PKD Regulates Membrane Fission to Generate TGN to Cell Surface Transport Carriers. Cold Spring Harb. Perspect. Biol. 2011, 3, a005280.
48. Yeaman, C.; Ayala, M. I.; Wright, J. R.; Bard, F.; Bossard, C.; Ang, A.; Maeda, Y.; Seufferlein, T.; Mellman, I.; Nelson, W. J.; Malhotra, V. Protein Kinase D Regulates Basolateral Membrane Protein Exit From Trans-Golgi Network. Nat. Cell Biol. 2004, 6, 106-112.
49. Bisbal, M.; Conde, C.; Donoso, M.; Bollati, F.; Sesma, J.; Quiroga, S.; Díaz Añel, A. M.; Malhotra, V.; Marzolo, M. P.; Cáceres, A. Protein Kinase D Regulates Trafficking of Dendritic Membrane Proteins in Developing Neurons. J. Neurosci. 2008, 28, 9297-9308.
50. Masu, M.; Tanabe, Y.; Tsuchida, K.; Shigemoto, R.; Nakanishi, S. Sequence and Expression of a Metabotropic Glutamate Receptor. Nature 1991, 49, 760-765.
51. Valenti, O.; Conn, P. J.; Marino, M. J. Distinct Physiological Roles of the Gq-Coupled Metabotropic Glutamate Receptors Co-Expressed in the Same Neuronal Populations. J. Cell Physiol. 2002, 191, 125-137.
52. Dhami, G. K.; Ferguson, S. S. G. Regulation of Metabotropic Glutamate Receptor Signaling, Desensitization and Endo-cytosis. Pharmacol. Ther. 2006, 111, 260-271.
53. Willard, S. S.; Koochekpour, S. Glutamate Signaling in Benign and Malignant Disorders: Current Status, Future Perspectives, and Therapeutic Implications. Int. J. Biol. Sci. 2013, 9, 728-742.
54. Wang, H.; Rong, G.; Yan, B.; Reinhard, B. M. Optical Sizing of Immunolabel Clusters through Multispectral Plasmon Coupling Microscopy. Nano Lett. 2011, 11, 498-504.
55. Aaron, J.; Nitin, N.; Travis, K.; Kumar, S.; Collier, T.; Park, S. Y.; Jose-Yacamán, M.; Coghlan, L; Follen, M.; Richards-Kortum, R.; et al. Plasmon Resonance Coupling of Metal Nanoparticles for Molecular Imaging of Carcinogenesis in Vivo. J. Biomed. Opt. 2007, 12, 034007.
56. Fraire, J. C; Pérez, L. A.; Coronado, E. A. Cluster Size Effects in the SERS Response of Ag and Au Nanoparticle Aggregates: Experimental and Theoretical Insight. J. Phys. Chem. C 2013, 117, 23090-23107.
57. Luján, R.; Roberts, J. D. B.; Shigemoto, R.; Ohishi, H.; Somogyi, P. Differential Plasma Membrane Distribution of Metabotropic Glutamate Receptors mGluR1a, mGluR2 and mGluR5, Relative to Neurotransmitter Release Sites. J. Chem. Neuroanat. 1997, 13, 219-241.
58. Garraleta, B. C; Norton, P. R.; Lagugné-Labarthet, F. SERS Detection of Streptavidin/Biotin Monolayer Assemblies. Langmuir 2011, 27, 1494-1498.
59. Ringler, M.; Klar, T. A.; Schwemer, A.; Susha, A. S.; Stehr, J.; Raschke, G.; Funk, S.; Borowski, M.; Nichtl, A.; Kulrzinger, K.; Phillips, R. T.; Feldman, J. Moving Nanoparticles with Raman Scattering. Nano Lett. 2007, 7, 2753-2757.
60. Barth, A.; Zscherp, C. What Vibrations Tell Us about Proteins. Q. Rev. Biophys. 2002, 35, 369-430.
61. Le Ru, E.; Etchegoin, P. G. Principles of Surface Enhanced Raman Spectroscopy, Vol. 1; Elsevier: Amsterdam, 2009.
62. Moskovits, M. Persistent Misconceptions Regarding SERS. Phys. Chem. Chem. Phys. 2013, 15, 5301-5311.
63. Tamaru, H.; Kuwata, H.; Miyazaki, H. T.; Miyano, K. Resonant Light Scattering from Individual Ag Nanoparticles and Particle Pairs. Appl. Phys. Lett. 2002, 80, 1826-1828.
64. Kunda, P.; Paglini, G.; Quiroga, S.; Kosik, K.; Cáceres, A. Evidence for the Involvement of Tiam-1 in Axon Formation. J. Neurosci. 2001, 21, 2361-2372.
65. Rosso, S.; Bollati, F.; Bisbal, M.; Peretti, D.; Sumi, T.; Nakamura, T.; Quiroga, S.; Ferreira, A.; Cáceres, A. LIMK1 Regulates Golgi Dynamics, Traffic of Golgiderived Vesicles, and Process Extension in Primary Cultured Neurons. Mol. Biol. Cell 2004, 15, 3433-3449.
66. Jeyifous, O.; Waites, C. L; Specht, C. G.; Fujisawa, S.; Schubert, M.; Lin, E. I.; Marshall, J.; Aoki, C; de Silva, T.; Montgomery, J. M.; et al. SAP97 and CASK Mediate Sorting of NMDA Receptors through a Previously Unknown Secretory Pathway. Nat. Neurosci. 2009, 12, 1011-1019.
67. Encina, E. R.; Coronado, E. A. On the Far Field Optical Properties of Ag-Au Nanosphere Pairs. J. Phys. Chem. C 2010, 114, 16278-16284.
68. Encina, E. R.; Coronado, E. A. Plasmon Coupling in Silver Nanosphere Pairs. J. Phys. Chem. C 2010, 114, 3918-3923.
69. Encina, E. R.; Coronado, E. A. Near Field Enhancement in Ag Au Nanospheres Heterodimers. J. Phys. Chem. C 2011, 115, 15908-15914.
70. Palik, E. D. Handbook of Optical Constants of Solids; Academic Press: New York, 1985.