In vivo imaging of the morphology and changes in pH along the gastrointestinal tract of Japanese medaka by photonic band-gap hydrogel microspheres.

Colloidal crystalline microspheres with photonic band-gap properties responsive to media pH have been developed for in vivo imaging purposes. These colloidal crystalline microspheres were constructed from monodispersed core-shell nano-size particles with poly(styrene-co-acrylic acid) (PS-co-PAA) cores and poly(acrylic acid-co-N-isopropylacrylamide) (PAA-co-PNIPAM) hydrogel shells cross-linked by N,N'-methylenebisacrylamide. A significant shift in the photonic band-gap properties of these colloidal crystalline microspheres was observed in the pH range of 4-5. This was caused by the discontinuous volume phase transition of the hydrogel coating, due to the protonation/deprotonation of its acrylic acid moieties, on the core-shell nano-sized particles within the microspheres. The in vivo imaging capability of these pH-responsive photonic microspheres was demonstrated on a test organism - Japanese medaka, Oryzia latipes - in which the morphology and change in pH along their gastrointestinal (GI) tracts were revealed under an ordinary optical microscope. This work illustrates the potential of stimuli-responsive photonic band-gap materials in tissue-/organ-level in vivo bio-imaging.

[1]  Toyoichi Tanaka.  Collapse of Gels and the Critical Endpoint , 1978 .

[2]  M. Villiger,et al.  Towards high resolution optical imaging of beta cells in vivo. , 2010, Current pharmaceutical design.

[3]  M. Westerfield,et al.  The zebrafish : biology , 1999 .

[4]  Marcelino Bernardo,et al.  An enzymatically activated fluorescence probe for targeted tumor imaging. , 2007, Journal of the American Chemical Society.

[5]  R. Weissleder,et al.  Fluorescence imaging with near-infrared light: new technological advances that enable in vivo molecular imaging , 2002, European Radiology.

[6]  R. Pereiro,et al.  Nanoparticles as fluorescent labels for optical imaging and sensing in genomics and proteomics , 2011, Analytical and bioanalytical chemistry.

[7]  S. Kullman,et al.  An in vivo Look at Vertebrate Liver Architecture: Three‐Dimensional Reconstructions from Medaka (Oryzias latipes) , 2007, Anatomical record.

[8]  Byron Ballou,et al.  Fluorescence imaging of tumors in vivo. , 2005, Current medicinal chemistry.

[9]  Kaler,et al.  A class of microstructured particles through colloidal crystallization , 2000, Science.

[10]  D. Pine,et al.  Photonic Crystals from Emulsion Templates , 2001 .

[11]  Sanford A. Asher,et al.  Photonic Crystal Chemical Sensors: pH and Ionic Strength , 2000 .

[12]  Kwangmeyung Kim,et al.  Nanoprobes for biomedical imaging in living systems , 2011 .

[13]  I. Rønnestad,et al.  Ontogeny of digestive tract functionality in Japanese flounder, Paralichthys olivaceus studied by in vivo microinjection: pH and assimilation of free amino acids , 2000, Fish Physiology and Biochemistry.

[14]  F. Moyano,et al.  Gut pH as a limiting factor for digestive proteolysis in cultured juveniles of the gilthead sea bream (Sparus aurata) , 2012, Fish Physiology and Biochemistry.

[15]  Lu Wang,et al.  pH responsive fluorescence nanoprobe imaging of tumors by sensing the acidic microenvironment , 2011 .

[16]  Erlong Zhang,et al.  A review of NIR dyes in cancer targeting and imaging. , 2011, Biomaterials.

[17]  Zhongze Gu,et al.  Rapid synthesis of monodisperse polymer spheres for self-assembled photonic crystals , 2007 .

[18]  Vibha Rani,et al.  Nanotechnology: Emerging Tool for Diagnostics and Therapeutics , 2011, Applied biochemistry and biotechnology.

[19]  Miguel Holgado,et al.  3D Long‐range ordering in ein SiO2 submicrometer‐sphere sintered superstructure , 1997 .

[20]  Dhananjay Dendukuri,et al.  A route to three-dimensional structures in a microfluidic device: stop-flow interference lithography. , 2007, Angewandte Chemie.

[21]  Howon Lee,et al.  Magnetochromatic microspheres: rotating photonic crystals. , 2009, Journal of the American Chemical Society.

[22]  T. Caykara,et al.  Network structure and swelling behavior of poly(acrylamide/crotonic acid) hydrogels in aqueous salt solutions , 2003 .

[23]  N. Madias,et al.  Management of life-threatening acid-base disorders. Second of two parts. , 1998, The New England journal of medicine.

[24]  Yukikazu Takeoka,et al.  Dual Tuning of the Photonic Band‐Gap Structure in Soft Photonic Crystals , 2009 .

[25]  A. Lu,et al.  Magnetic nanoparticles: synthesis, protection, functionalization, and application. , 2007, Angewandte Chemie.

[26]  Jan Wolber,et al.  Detecting tumor response to treatment using hyperpolarized 13C magnetic resonance imaging and spectroscopy , 2007, Nature Medicine.

[27]  Bo Meng,et al.  Ordered macroporous titania photonic balls by micrometer-scale spherical assembly templating , 2005 .

[28]  F. Beltram,et al.  Green fluorescent protein based pH indicators for in vivo use: a review , 2009, Analytical and bioanalytical chemistry.

[29]  Morteza Mahmoudi,et al.  Engineered nanoparticles for biomolecular imaging. , 2011, Nanoscale.

[30]  M. Schartl,et al.  Medaka — a model organism from the far east , 2002, Nature Reviews Genetics.

[31]  P. Flory.  Principles of polymer chemistry , 1953 .

[32]  R. Tsien,et al.  Fluorescent indicators for cytosolic calcium based on rhodamine and fluorescein chromophores. , 1989, The Journal of biological chemistry.

[33]  R. Weissleder,et al.  In vivo imaging of tumors with protease-activated near-infrared fluorescent probes , 1999, Nature Biotechnology.

[34]  P. Basser,et al.  Osmotic swelling of polyacrylate hydrogels in physiological salt solutions. , 2000, Biomacromolecules.

[35]  A. Neogi,et al.  Refractive Index Change Due to Volume-Phase Transition in Polyacrylamide Gel Nanospheres for Optoelectronics and Bio-photonics , 2009 .

[36]  G. Yi,et al.  Electrospray‐Assisted Fabrication of Uniform Photonic Balls , 2004 .

[37]  K. Dušek,et al.  Deformational, swelling, and potentiometric behavior of ionized poly(methacrylic acid) gels. I. Theory , 1975 .

[38]  Thierry Gacoin,et al.  Biological applications of rare-earth based nanoparticles. , 2011, ACS nano.

[39]  Hisataka Kobayashi,et al.  Toxicity of Organic Fluorophores Used in Molecular Imaging: Literature Review , 2009, Molecular imaging.

[40]  Shuming Nie,et al.  Molecular mapping of tumor heterogeneity on clinical tissue specimens with multiplexed quantum dots. , 2010, ACS nano.

[41]  R. Gillies,et al.  ©1999 Cancer Research Campaign Article no. bjoc.1998.0455 Enhancement of chemotherapy by manipulation of tumour pH , 2022 .

[42]  S. Sukhishvili,et al.  Poly(methacrylic acid) Hydrogel Films and Capsules: Response to pH and Ionic Strength, and Encapsulation of Macromolecules , 2006 .

[43]  V. Biju,et al.  Delivering quantum dots to cells: bioconjugated quantum dots for targeted and nonspecific extracellular and intracellular imaging. , 2010, Chemical Society reviews.

[44]  Ick Chan Kwon,et al.  pH-Sensitive nanoflash for tumoral acidic pH imaging in live animals. , 2010, Small.

[45]  A. R. Bausch,et al.  Colloidosomes: Selectively Permeable Capsules Composed of Colloidal Particles , 2002, Science.

[46]  Alexander M Seifalian,et al.  Fluorescence nanoparticles “quantum dots” as drug delivery system and their toxicity: a review , 2011, Journal of drug targeting.

[47]  Younan Xia,et al.  A THREE-DIMENSIONAL PHOTONIC CRYSTAL OPERATING IN THE VISIBLE REGION , 1999 .

[48]  M. Horn,et al.  Food habits, gut morphology and pH, and assimilation efficiency of the zebraperch Hermosilla azurea, an herbivorous kyphosid fish of temperate marine waters , 1998 .

[49]  A S K Dzik-Jurasz,et al.  Molecular imaging in vivo: an introduction. , 2003, The British journal of radiology.

[50]  Yang Li,et al.  Resonance scattering particles as biological nanosensors in vitro and in vivo. , 2012, Chemical Society reviews.

[51]  R.J. Gillies,et al.  pH imaging , 2004, IEEE Engineering in Medicine and Biology Magazine.

[52]  Y. Ishikawa,et al.  Medakafish as a model system for vertebrate developmental genetics. , 2000, BioEssays : news and reviews in molecular, cellular and developmental biology.

[53]  H. Takeda,et al.  Development of the endoderm and gut in medaka, Oryzias latipes , 2006, Development, growth & differentiation.

[54]  Chit Yaw Fu,et al.  Development of biocompatible SERS nanotag with increased stability by chemisorption of reporter molecule for in vivo cancer detection. , 2010, Biosensors & bioelectronics.

[55]  S. Gambhir,et al.  Quantum Dots for Live Cells, in Vivo Imaging, and Diagnostics , 2005, Science.

[56]  Jianping Gao,et al.  Multiresponsive Inverse‐Opal Hydrogels , 2007 .

[57]  Kevin D. Costa,et al.  Sessile Droplet Templating of Miniature Porous Hemispheres from Colloid Crystals , 2007 .

[58]  Leone Spiccia,et al.  Nanomaterials: Applications in Cancer Imaging and Therapy , 2011, Advanced materials.

[59]  W. M. Leevy,et al.  Optical imaging of mammary and prostate tumors in living animals using a synthetic near infrared zinc(II)-dipicolylamine probe for anionic cell surfaces. , 2010, Journal of the American Chemical Society.

[60]  Michal Ilavský,et al.  Effect of electrostatic interactions on phase transition in the swollen polymeric network , 1981 .

[61]  C. Fahrni,et al.  Metal Ion-Responsive Fluorescent Probes for Two-Photon Excitation Microscopy. , 2011, Chemistry of materials : a publication of the American Chemical Society.

[62]  S. Asher,et al.  Polymerized colloidal crystal hydrogel films as intelligent chemical sensing materials , 1997, Nature.

[63]  A. Cho.  Connecting the Dots to Custom Catalysts , 2003, Science.

[64]  Rebekah Drezek,et al.  In vivo biodistribution of nanoparticles. , 2011, Nanomedicine.

[65]  C. Wood,et al.  Acid–base responses to feeding and intestinal Cl– uptake in freshwater- and seawater-acclimated killifish, Fundulus heteroclitus, an agastric euryhaline teleost , 2010, Journal of Experimental Biology.

[66]  André C. Arsenault,et al.  Photonic-crystal full-colour displays , 2007 .

[67]  Zhizhong Wu,et al.  Structural color in porous, superhydrophilic, and self-cleaning SiO2/TiO2 Bragg stacks. , 2007, Small.

[68]  Masayoshi Watanabe,et al.  A thermally adjustable multicolor photochromic hydrogel. , 2007, Angewandte Chemie.

[69]  Hisashi Saito,et al.  Simple and precision design of porous gel as a visible indicator for ionic species and concentration. , 2003, Chemical communications.

[70]  Y. Lee,et al.  Effect of polyelectrolyte on the lower critical solution temperature of poly(N-isopropyl acrylamide) in the poly(NIPAAm-co-acrylic acid) hydrogel , 2000 .

[71]  F. Ojeda,et al.  Digestive mechanisms in Aplodactylus punctatus (Valenciennes): a temperate marine herbivorous fish , 1995 .

[72]  Kunio Furusawa,et al.  Assembly of Latex Particles by Using Emulsion Droplets as Templates. 1. Microstructured Hollow Spheres , 1996 .

[73]  A. Rózański,et al.  498. The dissociation constants of some symmetrically disubstituted succinic acids , 1959 .

[74]  Orlin D. Velev,et al.  Synthesis of Light‐Diffracting Assemblies from Microspheres and Nanoparticles in Droplets on a Superhydrophobic Surface , 2008 .

[75]  J. Fujimoto.  Optical coherence tomography for ultrahigh resolution in vivo imaging , 2003, Nature Biotechnology.

[76]  M. Yúfera,et al.  Changes in the gastrointestinal pH from larvae to adult in Senegal sole (Solea senegalensis) , 2007 .

[77]  S. Asher,et al.  Development of an intelligent polymerized crystalline colloidal array colorimetric reagent. , 2001, Analytical chemistry.

[78]  Venkataramanan Krishnaswamy,et al.  Radiologic and near-infrared/optical spectroscopic imaging: where is the synergy? , 2010, AJR. American journal of roentgenology.

[79]  S. Gambhir,et al.  Gold nanoparticles: a revival in precious metal administration to patients. , 2011, Nano letters.

[80]  Tristan Barrett,et al.  Selective molecular imaging of viable cancer cells with pH-activatable fluorescence probes , 2009, Nature Medicine.

[81]  Yadong Yin,et al.  Responsive photonic crystals. , 2011, Angewandte Chemie.

[82]  Masato Kinoshita,et al.  Medaka: Biology, Management, and Experimental Protocols , 2009 .

[83]  Lihui Weng,et al.  Investigation of pH sensitivity of poly(acrylic acid-co-acrylamide) hydrogel , 2003 .