Hình ảnh đa photon trong cơ thể về động học tế bào miễn dịch

Pflügers Archiv - Tập 468 - Trang 1793-1801 - 2016
Takaharu Okada1,2,3, Sonoko Takahashi1,2, Azusa Ishida1,2, Harumichi Ishigame1
1Laboratory for Tissue Dynamics, RIKEN Center for Integrative Medical Sciences, Yokohama, Japan
2Graduate School of Medical Life Science, Yokohama City University, Yokohama, Japan
3PRESTO, Japan Science and Technology Agency, Kawaguchi, Japan

Tóm tắt

Hình ảnh đa photon đã được sử dụng để phân tích động học tế bào miễn dịch in vivo trong suốt 15 năm qua. Đặc biệt, nó đã làm sâu sắc thêm sự hiểu biết về cách mà các đáp ứng miễn dịch được tổ chức thông qua sự di chuyển và tương tác của các tế bào miễn dịch. Trong bài tổng quan này, chúng tôi đầu tiên mô tả các tiến bộ kỹ thuật trong các nghiên cứu hình ảnh gần đây đã góp phần vào những phát hiện mới về việc điều hòa các đáp ứng miễn dịch và viêm. Hình ảnh đa màu sắc cải tiến về hành vi tế bào miễn dịch đã cho thấy rằng các tương tác của chúng được điều phối theo không gian và thời gian để đạt được miễn dịch hiệu quả và lâu dài. Việc sử dụng các protein huỳnh quang có thể kích hoạt bằng ánh sáng và biến đổi bằng ánh sáng đã tăng cường thời gian và khối lượng theo dõi tế bào, thậm chí cho phép phân tích di chuyển giữa các cơ quan của tế bào miễn dịch. Ngoài ra, việc hình dung sự kích hoạt tế bào miễn dịch bằng cách sử dụng cảm biến sinh học đối với nồng độ canxi bên trong tế bào và hoạt động của các phân tử tín hiệu đã bắt đầu cung cấp thêm những hiểu biết về cơ chế. Sau đó, chúng tôi cũng giới thiệu các phân tích hình ảnh gần đây về các tương tác giữa tế bào miễn dịch và tế bào không miễn dịch bao gồm tế bào nội mô, tế bào xơ, tế bào biểu mô và tế bào thần kinh. Chúng tôi cho rằng các nghiên cứu hình ảnh trong tương lai áp dụng các tiến bộ kỹ thuật cập nhật để phân tích các tương tác giữa tế bào miễn dịch và tế bào không miễn dịch sẽ rất quan trọng cho việc hiểu biết sinh lý học sâu sắc về hệ miễn dịch.

Từ khóa

#hình ảnh đa photon #tế bào miễn dịch #động học tế bào #tương tác tế bào #miễn dịch in vivo

Tài liệu tham khảo

Allen CD, Okada T, Cyster JG (2007) Germinal-center organization and cellular dynamics. Immunity 27:190–202 Allen CD, Okada T, Tang HL, Cyster JG (2007) Imaging of germinal center selection events during affinity maturation. Science 315:528–531 Ando R, Hama H, Yamamoto-Hino M, Mizuno H, Miyawaki A (2002) An optical marker based on the UV-induced green-to-red photoconversion of a fluorescent protein. Proc Natl Acad Sci U S A 99:12651–12656 Aoki K, Kamioka Y, Matsuda M (2013) Fluorescence resonance energy transfer imaging of cell signaling from in vitro to in vivo: basis of biosensor construction, live imaging, and image processing. Dev Growth Differ 55:515–522 Bajenoff M, Egen JG, Koo LY, Laugier JP, Brau F, Glaichenhaus N, Germain RN (2006) Stromal cell networks regulate lymphocyte entry, migration, and territoriality in lymph nodes. Immunity 25:989–1001 Bedoui S, Heath WR, Mueller SN (2016) CD4(+) T-cell help amplifies innate signals for primary CD8(+) T-cell immunity. Immunol Rev 272:52–64 Bousso P, Bhakta NR, Lewis RS, Robey E (2002) Dynamics of thymocyte-stromal cell interactions visualized by two-photon microscopy. Science 296:1876–1880 Chtanova T, Hampton HR, Waterhouse LA, Wood K, Tomura M, Miwa Y, Mackay CR, Brink R, Phan TG (2014) Real-time interactive two-photon photoconversion of recirculating lymphocytes for discontinuous cell tracking in live adult mice. J Biophotonics 7:425–433 Daniels NJ, Hyde E, Ghosh S, Seo K, Price KM, Hoshino K, Kaisho T, Okada T, Ronchese F (2016) Antigen-specific cytotoxic T lymphocytes target airway CD103+ and CD11b + dendritic cells to suppress allergic inflammation. Mucosal Immunol 9:229–239 Denk W, Svoboda K (1997) Photon upmanship: why multiphoton imaging is more than a gimmick. Neuron 18:351–357 Devi S, Li A, Westhorpe CL, Lo CY, Abeynaike LD, Snelgrove SL, Hall P, Ooi JD, Sobey CG, Kitching AR, Hickey MJ (2013) Multiphoton imaging reveals a new leukocyte recruitment paradigm in the glomerulus. Nat Med 19:107–112 Eickhoff S, Brewitz A, Gerner MY, Klauschen F, Komander K, Hemmi H, Garbi N, Kaisho T, Germain RN, Kastenmuller W (2015) Robust anti-viral immunity requires multiple distinct T cell-dendritic cell interactions. Cell 162:1322–1337 Farache J, Koren I, Milo I, Gurevich I, Kim KW, Zigmond E, Furtado GC, Lira SA, Shakhar G (2013) Luminal bacteria recruit CD103+ dendritic cells into the intestinal epithelium to sample bacterial antigens for presentation. Immunity 38:581–595 Gabanyi I, Muller PA, Feighery L, Oliveira TY, Costa-Pinto FA, Mucida D (2016) Neuro-immune interactions drive tissue programming in intestinal macrophages. Cell 164:378–391 Garrod KR, Moreau HD, Garcia Z, Lemaitre F, Bouvier I, Albert ML, Bousso P (2012) Dissecting T cell contraction in vivo using a genetically encoded reporter of apoptosis. Cell Rep 2:1438–1447 Germain RN, Robey EA, Cahalan MD (2012) A decade of imaging cellular motility and interaction dynamics in the immune system. Science 336:1676–1681 Gerner MY, Kastenmuller W, Ifrim I, Kabat J, Germain RN (2012) Histo-cytometry: a method for highly multiplex quantitative tissue imaging analysis applied to dendritic cell subset microanatomy in lymph nodes. Immunity 37:364–376 Gerner MY, Torabi-Parizi P, Germain RN (2015) Strategically localized dendritic cells promote rapid T cell responses to lymph-borne particulate antigens. Immunity 42:172–185 Ghigo C, Mondor I, Jorquera A, Nowak J, Wienert S, Zahner SP, Clausen BE, Luche H, Malissen B, Klauschen F, Bajenoff M (2013) Multicolor fate mapping of Langerhans cell homeostasis. J Exp Med 210:1657–1664 Green JA, Cyster JG (2012) S1PR2 links germinal center confinement and growth regulation. Immunol Rev 247:36–51 Greenberg ML, Weinger JG, Matheu MP, Carbajal KS, Parker I, Macklin WB, Lane TE, Cahalan MD (2014) Two-photon imaging of remyelination of spinal cord axons by engrafted neural precursor cells in a viral model of multiple sclerosis. Proc Natl Acad Sci U S A 111:E2349–E2355 Grigorova IL, Panteleev M, Cyster JG (2010) Lymph node cortical sinus organization and relationship to lymphocyte egress dynamics and antigen exposure. Proc Natl Acad Sci U S A 107:20447–20452 Grigorova IL, Schwab SR, Phan TG, Pham TH, Okada T, Cyster JG (2009) Cortical sinus probing, S1P1-dependent entry and flow-based capture of egressing T cells. Nat Immunol 10:58–65 Guan Y, Watson AJ, Marchiando AM, Bradford E, Shen L, Turner JR, Montrose MH (2011) Redistribution of the tight junction protein ZO-1 during physiological shedding of mouse intestinal epithelial cells. Am J Physiol Cell Physiol 300:C1404–C1414 Heath WR, Carbone FR (2009) Dendritic cell subsets in primary and secondary T cell responses at body surfaces. Nat Immunol 10:1237–1244 Heath WR, Carbone FR (2013) The skin-resident and migratory immune system in steady state and memory: innate lymphocytes, dendritic cells and T cells. Nat Immunol 14:978–985 Hiratsuka T, Fujita Y, Naoki H, Aoki K, Kamioka Y, Matsuda M (2015) Intercellular propagation of extracellular signal-regulated kinase activation revealed by in vivo imaging of mouse skin. Elife 4:e05178 Hong M, Jung E, Yang S, Jung W, Seong YJ, Park E, Bramos A, Kim KE, Lee S, Daghlian G, Seo JI, Choi I, Choi IS, Koh CJ, Kobielak A, Ying QL, Johnson M, Gardner D, Wong AK, Choi D, Hong YK (2016) Efficient assessment of developmental, surgical and pathological lymphangiogenesis using a lymphatic reporter mouse and its embryonic stem cells. PLoS One 11:e0157126 Hor JL, Whitney PG, Zaid A, Brooks AG, Heath WR, Mueller SN (2015) Spatiotemporally distinct interactions with dendritic cell subsets facilitates CD4+ and CD8+ T cell activation to localized viral infection. Immunity 43:554–565 Ibiza S, Garcia-Cassani B, Ribeiro H, Carvalho T, Almeida L, Marques R, Misic AM, Bartow-McKenney C, Larson DM, Pavan WJ, Eberl G, Grice EA, Veiga-Fernandes H (2016) Glial-cell-derived neuroregulators control type 3 innate lymphoid cells and gut defence. Nature 535:440–443 Jain R, Tikoo S, Weninger W (2016) Recent advances in microscopic techniques for visualizing leukocytes in vivo. F1000Res 5 Jarjour M, Jorquera A, Mondor I, Wienert S, Narang P, Coles MC, Klauschen F, Bajenoff M (2014) Fate mapping reveals origin and dynamics of lymph node follicular dendritic cells. J Exp Med 211:1109–1122 Kamioka Y, Sumiyama K, Mizuno R, Sakai Y, Hirata E, Kiyokawa E, Matsuda M (2012) Live imaging of protein kinase activities in transgenic mice expressing FRET biosensors. Cell Struct Funct 37:65–73 Kashem SW, Riedl MS, Yao C, Honda CN, Vulchanova L, Kaplan DH (2015) Nociceptive sensory fibers drive interleukin-23 production from CD301b+ dermal dendritic cells and drive protective cutaneous immunity. Immunity 43:515–526 Kitano M, Moriyama S, Ando Y, Hikida M, Mori Y, Kurosaki T, Okada T (2011) Bcl6 protein expression shapes pre-germinal center B cell dynamics and follicular helper T cell heterogeneity. Immunity 34:961–972 Kitano M, Yamazaki C, Takumi A, Ikeno T, Hemmi H, Takahashi N, Shimizu K, Fraser SE, Hoshino K, Kaisho T, Okada T (2016) Imaging of the cross-presenting dendritic cell subsets in the skin-draining lymph node. Proc Natl Acad Sci U S A 113:1044–1049 Kiyokawa E, Aoki K, Nakamura T, Matsuda M (2011) Spatiotemporal regulation of small GTPases as revealed by probes based on the principle of Forster Resonance Energy Transfer (FRET): implications for signaling and pharmacology. Annu Rev Pharmacol Toxicol 51:337–358 Kubo A, Nagao K, Yokouchi M, Sasaki H, Amagai M (2009) External antigen uptake by Langerhans cells with reorganization of epidermal tight junction barriers. J Exp Med 206:2937–2946 Le Borgne M, Raju S, Zinselmeyer BH, Le VT, Li J, Wang Y, Miller MJ, Shaw AS (2016) Real-time analysis of calcium signals during the early phase of T cell activation using a genetically encoded calcium biosensor. J Immunol 196:1471–1479 Liu D, Xu H, Shih C, Wan Z, Ma X, Ma W, Luo D, Qi H (2015) T-B-cell entanglement and ICOSL-driven feed-forward regulation of germinal centre reaction. Nature 517:214–218 Lodygin D, Odoardi F, Schlager C, Korner H, Kitz A, Nosov M, van den Brandt J, Reichardt HM, Haberl M, Flugel A (2013) A combination of fluorescent NFAT and H2B sensors uncovers dynamics of T cell activation in real time during CNS autoimmunity. Nat Med 19:784–790 Maeda H, Kowada T, Kikuta J, Furuya M, Shirazaki M, Mizukami S, Ishii M, Kikuchi K (2016) Real-time intravital imaging of pH variation associated with osteoclast activity. Nat Chem Biol 12:579–585 Marangoni F, Murooka TT, Manzo T, Kim EY, Carrizosa E, Elpek NM, Mempel TR (2013) The transcription factor NFAT exhibits signal memory during serial T cell interactions with antigen-presenting cells. Immunity 38:237–249 McDole JR, Wheeler LW, McDonald KG, Wang B, Konjufca V, Knoop KA, Newberry RD, Miller MJ (2012) Goblet cells deliver luminal antigen to CD103+ dendritic cells in the small intestine. Nature 483:345–349 Miller MJ, Wei SH, Cahalan MD, Parker I (2003) Autonomous T cell trafficking examined in vivo with intravital two-photon microscopy. Proc Natl Acad Sci U S A 100:2604–2609 Miller MJ, Wei SH, Parker I, Cahalan MD (2002) Two-photon imaging of lymphocyte motility and antigen response in intact lymph node. Science 296:1869–1873 Mionnet C, Sanos SL, Mondor I, Jorquera A, Laugier JP, Germain RN, Bajenoff M (2011) High endothelial venules as traffic control points maintaining lymphocyte population homeostasis in lymph nodes. Blood 118:6115–6122 Mizuno R, Kamioka Y, Kabashima K, Imajo M, Sumiyama K, Nakasho E, Ito T, Hamazaki Y, Okuchi Y, Sakai Y, Kiyokawa E, Matsuda M (2014) In vivo imaging reveals PKA regulation of ERK activity during neutrophil recruitment to inflamed intestines. J Exp Med 211:1123–1136 Mizuno R, Kamioka Y, Sakai Y, Matsuda M (2016) Visualization of signaling molecules during neutrophil recruitment in transgenic mice expressing FRET biosensors. Methods Mol Biol 1422:149–160 Moriyama S, Takahashi N, Green JA, Hori S, Kubo M, Cyster JG, Okada T (2014) Sphingosine-1-phosphate receptor 2 is critical for follicular helper T cell retention in germinal centers. J Exp Med 211:1297–1305 Mues M, Bartholomaus I, Thestrup T, Griesbeck O, Wekerle H, Kawakami N, Krishnamoorthy G (2013) Real-time in vivo analysis of T cell activation in the central nervous system using a genetically encoded calcium indicator. Nat Med 19:778–783 Natsuaki Y, Egawa G, Nakamizo S, Ono S, Hanakawa S, Okada T, Kusuba N, Otsuka A, Kitoh A, Honda T, Nakajima S, Tsuchiya S, Sugimoto Y, Ishii KJ, Tsutsui H, Yagita H, Iwakura Y, Kubo M, Ng L, Hashimoto T, Fuentes J, Guttman-Yassky E, Miyachi Y, Kabashima K (2014) Perivascular leukocyte clusters are essential for efficient activation of effector T cells in the skin. Nat Immunol 15:1064–1069 Ordovas-Montanes J, Rakoff-Nahoum S, Huang S, Riol-Blanco L, Barreiro O, von Andrian UH (2015) The regulation of immunological processes by peripheral neurons in homeostasis and disease. Trends Immunol 36:578–604 Patterson GH, Lippincott-Schwartz J (2002) A photoactivatable GFP for selective photolabeling of proteins and cells. Science 297:1873–1877 Pearson C, Thornton EE, McKenzie B, Schaupp AL, Huskens N, Griseri T, West N, Tung S, Seddon BP, Uhlig HH, Powrie F (2016) ILC3 GM-CSF production and mobilisation orchestrate acute intestinal inflammation. Elife 5:e10066 Pesic M, Bartholomaus I, Kyratsous NI, Heissmeyer V, Wekerle H, Kawakami N (2013) 2-photon imaging of phagocyte-mediated T cell activation in the CNS. J Clin Invest 123:1192–1201 Qi H, Egen JG, Huang AY, Germain RN (2006) Extrafollicular activation of lymph node B cells by antigen-bearing dendritic cells. Science 312:1672–1676 Riol-Blanco L, Ordovas-Montanes J, Perro M, Naval E, Thiriot A, Alvarez D, Paust S, Wood JN, von Andrian UH (2014) Nociceptive sensory neurons drive interleukin-23-mediated psoriasiform skin inflammation. Nature 510:157–161 Roediger B, Kyle R, Yip KH, Sumaria N, Guy TV, Kim BS, Mitchell AJ, Tay SS, Jain R, Forbes-Blom E, Chen X, Tong PL, Bolton HA, Artis D, Paul WE, Fazekas de St Groth B, Grimbaldeston MA, Le Gros G, Weninger W (2013) Cutaneous immunosurveillance and regulation of inflammation by group 2 innate lymphoid cells. Nat Immunol 14:564–573 Schiessl IM, Castrop H (2016) Deep insights: intravital imaging with two-photon microscopy. Pflugers Arch Schneider M, Barozzi S, Testa I, Faretta M, Diaspro A (2005) Two-photon activation and excitation properties of PA-GFP in the 720-920-nm region. Biophys J 89:1346–1352 Shulman Z, Gitlin AD, Targ S, Jankovic M, Pasqual G, Nussenzweig MC, Victora GD (2013) T follicular helper cell dynamics in germinal centers. Science 341:673–677 Shulman Z, Gitlin AD, Weinstein JS, Lainez B, Esplugues E, Flavell RA, Craft JE, Nussenzweig MC (2014) Dynamic signaling by T follicular helper cells during germinal center B cell selection. Science 345:1058–1062 Siffrin V, Radbruch H, Glumm R, Niesner R, Paterka M, Herz J, Leuenberger T, Lehmann SM, Luenstedt S, Rinnenthal JL, Laube G, Luche H, Lehnardt S, Fehling HJ, Griesbeck O, Zipp F (2010) In vivo imaging of partially reversible th17 cell-induced neuronal dysfunction in the course of encephalomyelitis. Immunity 33:424–436 Snippert HJ, van der Flier LG, Sato T, van Es JH, van den Born M, Kroon-Veenboer C, Barker N, Klein AM, van Rheenen J, Simons BD, Clevers H (2010) Intestinal crypt homeostasis results from neutral competition between symmetrically dividing Lgr5 stem cells. Cell 143:134–144 Stark K, Eckart A, Haidari S, Tirniceriu A, Lorenz M, von Bruhl ML, Gartner F, Khandoga AG, Legate KR, Pless R, Hepper I, Lauber K, Walzog B, Massberg S (2013) Capillary and arteriolar pericytes attract innate leukocytes exiting through venules and ‘instruct’ them with pattern-recognition and motility programs. Nat Immunol 14:41–51 Stoll S, Delon J, Brotz TM, Germain RN (2002) Dynamic imaging of T cell-dendritic cell interactions in lymph nodes. Science 296:1873–1876 Suan D, Nguyen A, Moran I, Bourne K, Hermes JR, Arshi M, Hampton HR, Tomura M, Miwa Y, Kelleher AD, Kaplan W, Deenick EK, Tangye SG, Brink R, Chtanova T, Phan TG (2015) T follicular helper cells have distinct modes of migration and molecular signatures in naive and memory immune responses. Immunity 42:704–718 Sujino T, London M, Hoytema van Konijnenburg DP, Rendon T, Buch T, Silva HM, Lafaille JJ, Reis BS, Mucida D (2016) Tissue adaptation of regulatory and intraepithelial CD4(+) T cells controls gut inflammation. Science 352:1581–1586 Tas JM, Mesin L, Pasqual G, Targ S, Jacobsen JT, Mano YM, Chen CS, Weill JC, Reynaud CA, Browne EP, Meyer-Hermann M, Victora GD (2016) Visualizing antibody affinity maturation in germinal centers. Science 351:1048–1054 Thestrup T, Litzlbauer J, Bartholomaus I, Mues M, Russo L, Dana H, Kovalchuk Y, Liang Y, Kalamakis G, Laukat Y, Becker S, Witte G, Geiger A, Allen T, Rome LC, Chen TW, Kim DS, Garaschuk O, Griesinger C, Griesbeck O (2014) Optimized ratiometric calcium sensors for functional in vivo imaging of neurons and T lymphocytes. Nat Methods 11:175–182 Tomura M, Hata A, Matsuoka S, Shand FH, Nakanishi Y, Ikebuchi R, Ueha S, Tsutsui H, Inaba K, Matsushima K, Miyawaki A, Kabashima K, Watanabe T, Kanagawa O (2014) Tracking and quantification of dendritic cell migration and antigen trafficking between the skin and lymph nodes. Sci Rep 4:6030 Tomura M, Honda T, Tanizaki H, Otsuka A, Egawa G, Tokura Y, Waldmann H, Hori S, Cyster JG, Watanabe T, Miyachi Y, Kanagawa O, Kabashima K (2010) Activated regulatory T cells are the major T cell type emigrating from the skin during a cutaneous immune response in mice. J Clin Invest 120:883–893 Tsutsui H, Karasawa S, Shimizu H, Nukina N, Miyawaki A (2005) Semi-rational engineering of a coral fluorescent protein into an efficient highlighter. EMBO Rep 6:233–238 Veiga-Fernandes H, Mucida D (2016) Neuro-immune interactions at barrier surfaces. Cell 165:801–811 Victora GD, Nussenzweig MC (2012) Germinal centers. Annu Rev Immunol 30:429–457 Victora GD, Schwickert TA, Fooksman DR, Kamphorst AO, Meyer-Hermann M, Dustin ML, Nussenzweig MC (2010) Germinal center dynamics revealed by multiphoton microscopy with a photoactivatable fluorescent reporter. Cell 143:592–605 Wei SH, Rosen H, Matheu MP, Sanna MG, Wang SK, Jo E, Wong CH, Parker I, Cahalan MD (2005) Sphingosine 1-phosphate type 1 receptor agonism inhibits transendothelial migration of medullary T cells to lymphatic sinuses. Nat Immunol 6:1228–1235 Wei SH, Safrina O, Yu Y, Garrod KR, Cahalan MD, Parker I (2007) Ca2+ signals in CD4+ T cells during early contacts with antigen-bearing dendritic cells in lymph node. J Immunol 179:1586–1594 Whitaker M (2010) Genetically encoded probes for measurement of intracellular calcium. Methods Cell Biol 99:153–182 Williams EK, Chang RB, Strochlic DE, Umans BD, Lowell BB, Liberles SD (2016) Sensory neurons that detect stretch and nutrients in the digestive system. Cell 166:209–221 Yasuda R (2012) Imaging intracellular signaling using two-photon fluorescent lifetime imaging microscopy. Cold Spring Harb Protoc 2012:1121–1128 Yoshikawa S, Usami T, Kikuta J, Ishii M, Sasano T, Sugiyama K, Furukawa T, Nakasho E, Takayanagi H, Tedder TF, Karasuyama H, Miyawaki A, Adachi T (2016) Intravital imaging of Ca(2+) signals in lymphocytes of Ca(2+) biosensor transgenic mice: indication of autoimmune diseases before the pathological onset. Sci Rep 6:18738