Near-infrared photoactivatable control of Ca2+ signaling and optogenetic immunomodulation

eLife

Volumn 4, Issue DECEMBER2015, 2015, Pages

  He, Lian ^a   Zhang, Yuanwei ^b   Ma, Guolin ^a   Tan, Peng ^a   Li, Zhanjun ^b   Zang, Shengbing ^a   Wu, Xiang ^b   Jing, Ji ^a   Fang, Shaohai ^a   Zhou, Lijuan ^c   Wang, Youjun ^c   Huang, Yun ^a   Hogan, Patrick G ^d   Han, Gang ^b   Zhou, Yubin ^a,e  

^a TEXAS A AND M HEALTH SCIENCE CENTER   (United States)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^c BEIJING NORMAL UNIVERSITY   (China)

^d LA JOLLA INSTITUTE FOR ALLERGY AND IMMUNOLOGY   (United States)

^e TEXAS A M COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; INTERLEUKIN 2; SODIUM; STROMAL INTERACTION MOLECULE 1; T LYMPHOCYTE RECEPTOR; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR NFAT;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOLUMINESCENCE; BONE MARROW DERIVED DENDRITIC CELL; CALCIUM SIGNALING; CD4+ T LYMPHOCYTE; CELL ISOLATION; CELL TRANSFER; CONTROLLED STUDY; ELECTROPHYSIOLOGY; ENZYME LINKED IMMUNOSORBENT ASSAY; ESCHERICHIA COLI; FEMALE; FLUORESCENCE IMAGING; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; HISTOLOGY; HUMAN; HUMAN CELL; IMMUNOMODULATION; IMMUNOPRECIPITATION; INFRARED SPECTROSCOPY; MICROSCOPY; NEAR INFRARED IMAGING SYSTEM; NONHUMAN; OPTOGENETICS; PHOTOSTIMULATION; PHYSICAL PARAMETERS; PROTEIN EXPRESSION; QUANTUM EFFICIENCY; REAL TIME POLYMERASE CHAIN REACTION; T LYMPHOCYTE ACTIVATION; TOTAL INTERNAL REFLECTION FLUORESCENCE MICROSCOPY; TUMOR GROWTH; ANIMAL; DENDRITIC CELL; DISEASE MODEL; IMMUNOLOGY; INFRARED RADIATION; MACROPHAGE; MELANOMA; MOUSE; PHYSIOLOGY; PROCEDURES; RADIATION RESPONSE; T LYMPHOCYTE;

ANIMALS; CALCIUM SIGNALING; DENDRITIC CELLS; DISEASE MODELS, ANIMAL; IMMUNOMODULATION; INFRARED RAYS; MACROPHAGES; MELANOMA; MICE; OPTOGENETICS; T-LYMPHOCYTES;

EID: 84955285793     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.10024.001     Document Type: Article

References (58)

1. Briles EB, Kornfeld S. 1978. Isolation and metastatic properties of detachment variants of B16 melanoma cells. Journal of the National Cancer Institute 60:1217-1222.
2. Chen G, Qiu H, Prasad PN, Chen X. 2014. Upconversion nanoparticles: design, nanochemistry, and applications in theranostics. Chemical Reviews 114:5161-5214. doi: 10.1021/cr400425h
3. Chen TW, Wardill TJ, Sun Y, Pulver SR, Renninger SL, Baohan A, Schreiter ER, Kerr RA, Orger MB, Jayaraman V, Looger LL, Svoboda K, Kim DS. 2013. Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 499:295-300. doi: 10.1038/nature12354
4. Christie JM, Salomon M, Nozue K, Wada M, Briggs WR. 1999. LOV (light, oxygen, or voltage) domains of the blue-light photoreceptor phototropin (nph1): binding sites for the chromophore flavin mononucleotide. Proceedings of the National Academy of Sciences of the United States of America 96:8779-8783. doi: 10.1073/ pnas.96.15.8779
5. Clarke SR, Barnden M, Kurts C, Carbone FR, Miller JF, Heath WR. 2000. Characterization of the ovalbumin- specific TCR transgenic line OT-i: MHC elements for positive and negative selection. Immunology and Cell Biology 78:110-117. doi: 10.1046/j.1440-1711.2000.00889.x
6. Czerniecki BJ, Carter C, Rivoltini L, Koski GK, Kim HI, Weng DE, Roros JG, Hijazi YM, Xu S, Rosenberg SA, Cohen PA. 1997. Calcium ionophore-treated peripheral blood monocytes and dendritic cells rapidly display characteristics of activated dendritic cells. Journal of Immunology 159:3823-3837.
7. de Felipe P, Luke GA, Hughes LE, Gani D, Halpin C, Ryan MD. 2006. E unum pluribus: multiple proteins from a self-processing polyprotein. Trends in Biotechnology 24:68-75. doi: 10.1016/j.tibtech.2005.12.006
8. Dolmetsch RE, Xu K, Lewis RS. 1998. Calcium oscillations increase the efficiency and specificity of gene expression. Nature 392:933-936. doi: 10.1038/31960
9. Dong A, Ye X, Chen J, Kang Y, Gordon T, Kikkawa JM, Murray CB. 2011. A generalized ligand-exchange strategy enabling sequential surface functionalization of colloidal nanocrystals. Journal of the American Chemical Society 133:998-1006. doi: 10.1021/ja108948z
10. Falo LD, Kovacsovics-Bankowski M, Thompson K, Rock KL. 1995. Targeting antigen into the phagocytic pathway in vivo induces protective tumour immunity. Nature Medicine 1:649-653. doi: 10.1038/nm0795-649
11. Fenno L, Yizhar O, Deisseroth K. 2011. The development and application of optogenetics. Annual Review of Neuroscience 34:389-412. doi: 10.1146/annurev-neuro-061010-113817
12. Fidler IJ. 1975. Biological behavior of malignant melanoma cells correlated to their survival in vivo. Cancer Research 35:218-224.
13. Félix R, Crottès D, Delalande A, Fauconnier J, Lebranchu Y, Le Guennec JY, Velge-Roussel F. 2013. The orai-1 and STIM-1 complex controls human dendritic cell maturation. PloS One 8:e61595 doi: 10.1371/journal.pone. 0061595
14. Gnach A, Lipinski T, Bednarkiewicz A, Rybka J, Capobianco JA. 2015. Upconverting nanoparticles: assessing the toxicity. Chemical Society Reviews 44:1561-1584. doi: 10.1039/c4cs00177j
15. Harper SM, Neil LC, Gardner KH. 2003. Structural basis of a phototropin light switch. Science 301:1541-1544. doi: 10.1126/science.1086810
16. Hogan PG, Lewis RS, Rao A. 2010. Molecular basis of calcium signaling in lymphocytes: STIM and ORAI. Annual Review of Immunology 28:491-533. doi: 10.1146/annurev.immunol.021908.132550
17. Hogquist KA, Jameson SC, Heath WR, Howard JL, Bevan MJ, Carbone FR. 1994. T cell receptor antagonist peptides induce positive selection. Cell 76:17-27. doi: 10.1016/0092-8674(94)90169-4
18. Horng T. 2014. Calcium signaling and mitochondrial destabilization in the triggering of the NLRP3 inflammasome. Trends in Immunology 35:253-261. doi: 10.1016/j.it.2014.02.007
19. Hsu S-F, O'Connell PJ, Klyachko VA, Badminton MN, Thomson AW, Jackson MB, Clapham DE, Ahern GP. 2001. Fundamental Ca2+ signaling mechanisms in mouse dendritic cells: CRAC is the major Ca2+ entry pathway. The Journal of Immunology 166:6126-6133. doi: 10.4049/jimmunol.166.10.6126
20. Inoue M, Takeuchi A, Horigane S, Ohkura M, Gengyo-Ando K, Fujii H, Kamijo S, Takemoto-Kimura S, Kano M, Nakai J, Kitamura K, Bito H. 2015. Rational design of a high-affinity, fast, red calcium indicator r-CaMP2. Nature Methods 12:64-70. doi: 10.1038/nmeth.3185
21. Inoue T, Heo WD, Grimley JS, Wandless TJ, Meyer T. 2005. An inducible translocation strategy to rapidly activate and inhibit small GTPase signaling pathways. Nature Methods 2:415-418. doi: 10.1038/nmeth763
22. Koski GK, Schwartz GN, Weng DE, Czerniecki BJ, Carter C, Gress RE, Cohen PA. 1999. Calcium mobilization in human myeloid cells results in acquisition of individual dendritic cell-like characteristics through discrete signaling pathways. Journal of Immunology 163:82-92.
23. Lee GS, Subramanian N, Kim AI, Aksentijevich I, Goldbach-Mansky R, Sacks DB, Germain RN, Kastner DL, Chae JJ. 2012. The calcium-sensing receptor regulates the NLRP3 inflammasome through Ca2+ and cAMP. Nature 492:123-127. doi: 10.1038/nature11588
24. Ma G, Wei M, He L, Liu C, Wu B, Zhang SL, Jing J, Liang X, Senes A, Tan P, Li S, Sun A, Bi Y, Zhong L, Si H, Shen Y, Li M, Lee M-S, Zhou W, Wang J, Wang Y, Zhou Y. 2015. Inside-out Ca2+ signalling prompted by STIM1 conformational switch. Nature Communications 6:7826. doi: 10.1038/ncomms8826
25. Mai HX, Zhang YW, Si R, Yan ZG, Sun LD, You LP, Yan CH. 2006. High-quality sodium rare-earth fluoride nanocrystals: controlled synthesis and optical properties. Journal of the American Chemical Society 128:6426-6436. doi: 10.1021/ja060212h
26. Matzner N, Zemtsova IM, Nguyen TX, Duszenko M, Shumilina E, Lang F. 2008. Ion channels modulating mouse dendritic cell functions. Journal of Immunology 181:6803-6809. doi: 10.4049/jimmunol.181.10.6803
27. Mayordomo JI, Zorina T, Storkus WJ, Zitvogel L, Celluzzi C, Falo LD, Melief CJ, Ildstad ST, Kast WM, Deleo AB.1995. Bone marrow-derived dendritic cells pulsed with synthetic tumour peptides elicit protective and therapeutic antitumour immunity. Nature Medicine 1:1297-1302. doi: 10.1038/nm1295-1297
28. Morgan RA, Yang JC, Kitano M, Dudley ME, Laurencot CM, Rosenberg SA. 2010. Case report of a serious adverse event following the administration of T cells transduced with a chimeric antigen receptor recognizing ERBB2. Molecular Therapy 18:843-851. doi: 10.1038/mt.2010.24
29. Murakami T, Ockinger J, Yu J, Byles V, McColl A, Hofer AM, Horng T. 2012. Critical role for calcium mobilization in activation of the NLRP3 inflammasome. Proceedings of the National Academy of Sciences of the United States of America 109:11282-11287. doi: 10.1073/pnas.1117765109
30. Muro E, Pons T, Lequeux N, Fragola A, Sanson N, Lenkei Z, Dubertret B. 2010. Small and stable sulfobetaine zwitterionic quantum dots for functional live-cell imaging. Journal of the American Chemical Society 132:4556-4557. doi: 10.1021/ja1005493
31. Müller MR, Rao A. 2010. NFAT, immunity and cancer: a transcription factor comes of age. Nature Reviews Immunology 10:645-656. doi: 10.1038/nri2818
32. Ostrowski AD, Chan EM, Gargas DJ, Katz EM, Han G, Schuck PJ, Milliron DJ, Cohen BE. 2012. Controlled synthesis and single-particle imaging of bright, sub-10 nm lanthanide-doped upconverting nanocrystals. ACS Nano 6:2686-2692. doi: 10.1021/nn3000737
33. Overwijk WW, Restifo NP. 2001. B16 as a mouse model for human melanoma. Current Protocols in Immunology 21. doi: 10.1002/0471142735.im2001s39
34. Palucka K, Banchereau J. 2012. Cancer immunotherapy via dendritic cells. Nature Reviews Cancer 12:265-277. doi: 10.1038/nrc3258
35. Parekh AB. 2008. Ca2+ microdomains near plasma membrane Ca2+ channels: impact on cell function. The Journal of Physiology 586:3043-3054. doi: 10.1113/jphysiol.2008.153460
36. Park CY, Hoover PJ, Mullins FM, Bachhawat P, Covington ED, Raunser S, Walz T, Garcia KC, Dolmetsch RE, Lewis RS. 2009. STIM1 clusters and activates CRAC channels via direct binding of a cytosolic domain to Orai1. Cell 136:876-890. doi: 10.1016/j.cell.2009.02.014
37. Pham E, Mills E, Truong K. 2011. A synthetic photoactivated protein to generate local or global Ca(2+) signals. Chemistry & Biology 18:880-890. doi: 10.1016/j.chembiol.2011.04.014
38. Prakriya M, Lewis RS. 2015. Store-operated calcium channels. Physiological Reviews 95:1383-1436. doi: 10. 1152/physrev.00020.2014
39. Punjabi A, Wu X, Tokatli-Apollon A, El-Rifai M, Lee H, Zhang Y, Wang C, Liu Z, Chan EM, Duan C, Han G. 2014. Amplifying the red-emission of upconverting nanoparticles for biocompatible clinically used prodrug-induced photodynamic therapy. ACS Nano 8:10621-10630. doi: 10.1021/nn505051d
40. Restifo NP, Dudley ME, Rosenberg SA. 2012. Adoptive immunotherapy for cancer: harnessing the T cell response. Nature Reviews Immunology 12:269-281. doi: 10.1038/nri3191
41. Schmidt TG, Skerra A. 2007. The strep-tag system for one-step purification and high-affinity detection or capturing of proteins. Nature Protocols 2:1528-1535. doi: 10.1038/nprot.2007.209
42. Shen J, Zhao L, Han G. 2013. Lanthanide-doped upconverting luminescent nanoparticle platforms for optical imaging-guided drug delivery and therapy. Advanced Drug Delivery Reviews 65:744-755. doi: 10.1016/j.addr. 2012.05.007
43. Shifrin AL, Auricchio A, Yu QC, Wilson J, Raper SE. 2001. Adenoviral vector-mediated insulin gene transfer in the mouse pancreas corrects streptozotocin-induced hyperglycemia. Gene Therapy 8:1480-1489. doi: 10.1038/sj. gt.3301544
44. Soboloff J, Rothberg BS, Madesh M, Gill DL. 2012. STIM proteins: dynamic calcium signal transducers. Nature Reviews. Molecular Cell Biology 13:549-565. doi: 10.1038/nrm3414
45. Stanley SA, Gagner JE, Damanpour S, Yoshida M, Dordick JS, Friedman JM. 2012. Radio-wave heating of iron oxide nanoparticles can regulate plasma glucose in mice. Science 336:604-608. doi: 10.1126/science.1216753
46. Strickland D, Yao X, Gawlak G, Rosen MK, Gardner KH, Sosnick TR. 2010. Rationally improving LOV domain- based photoswitches. Nature Methods 7:623-626. doi: 10.1038/nmeth.1473
47. Sun Y, Feng W, Yang P, Huang C, Li F. 2015. The biosafety of lanthanide upconversion nanomaterials. Chemical Society Reviews 44:1509-1525. doi: 10.1039/c4cs00175c
48. Wang X, Wang Y, Zhou Y, Hendron E, Mancarella S, Andrake MD, Rothberg BS, Soboloff J, Gill DL. 2014. Distinct orai-coupling domains in STIM1 and STIM2 define the orai-activating site. Nature Communications 5.
49. Wu J, Liu L, Matsuda T, Zhao Y, Rebane A, Drobizhev M, Chang YF, Araki S, Arai Y, March K, Hughes TE, Sagou K, Miyata T, Nagai T, Li WH, Campbell RE. 2013. Improved orange and red ca(2)+/- indicators and photophysical considerations for optogenetic applications. ACS Chemical Neuroscience 4:963-972. doi: 10. 1021/cn400012b
50. Wu S, Han G, Milliron DJ, Aloni S, Altoe V, Talapin DV, Cohen BE, Schuck PJ. 2009. Non-blinking and photostable upconverted luminescence from single lanthanide-doped nanocrystals. Proceedings of the National Academy of Sciences of the United States of America 106:10917-10921. doi: 10.1073/pnas. 0904792106
51. Wu X, Chen G, Shen J, Li Z, Zhang Y, Han G. 2015. Upconversion nanoparticles: a versatile solution to multiscale biological imaging. Bioconjugate Chemistry 26:166-175. doi: 10.1021/bc5003967
52. Wu YI, Frey D, Lungu OI, Jaehrig A, Schlichting I, Kuhlman B, Hahn KM. 2009. A genetically encoded photoactivatable rac controls the motility of living cells. Nature 461:104-108. doi: 10.1038/nature08241
53. Yao X, Rosen MK, Gardner KH. 2008. Estimation of the available free energy in a LOV2-j alpha photoswitch. Nature Chemical Biology 4:491-497. doi: 10.1038/nchembio.99
54. Yuan JP, Zeng W, Dorwart MR, Choi YJ, Worley PF, Muallem S. 2009. SOAR and the polybasic STIM1 domains gate and regulate orai channels. Nature Cell Biology 11:337-343. doi: 10.1038/ncb1842
55. Zhou Y, Meraner P, Kwon HT, Machnes D, Oh-hora M, Zimmer J, Huang Y, Stura A, Rao A, Hogan PG. 2010a. STIM1 gates the store-operated calcium channel ORAI1 . Nature Structural and Molecular Biology 17:112-116. doi: 10.1038/nsmb.1724
56. Zhou Y, Ramachandran S, Oh-hora M, Rao A, Hogan PG. 2010b. Pore architecture of the ORAI1 store-operated calcium channel. Proceedings of the National Academy of Sciences of the United States of America 107:4896-4901. doi: 10.1073/pnas.1001169107
57. Zhou Y, Srinivasan P, Razavi S, Seymour S, Meraner P, Gudlur A, Stathopulos PB, Ikura M, Rao A, Hogan PG.2013. Initial activation of STIM1, the regulator of store-operated calcium entry. Nature Structural & Molecular Biology 20:973-981. doi: 10.1038/nsmb.2625
58. Zweifach A, Lewis RS. 1993. Mitogen-regulated Ca2+ current of T lymphocytes is activated by depletion of intracellular Ca2+ stores. Proceedings of the National Academy of Sciences of the United States of America 90: 6295-6299. doi: 10.1073/pnas.90.13.6295