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Frontiers of Optoelectronics

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Front. Optoelectron.    2015, Vol. 8 Issue (2) : 141-151    https://doi.org/10.1007/s12200-014-0415-5
REVIEW ARTICLE
Two-photon microscopy in pre-clinical and clinical cancer research
Jun LIU()
OptiMedic Technologies, Inc., Foshan 528200, China
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Abstract

The applications of two-photon microscopy (TPM) on pre-clinical and clinical study of human cancer and diseases are reviewed in this paper. First, the principle of two-photon excitation (TPE) is introduced. The resulting advantages of TPM for imaging studies of animal models and human samples are then elaborated. Subsequently, the applications of TPM on various aspects of tumor studies, including tumor angiogenesis, invasion and metastasis, tumor microenvironment and metabolism are introduced. Furthermore, studies of TPM on clinical human skin biopsy and the development of two-photon microendoscopy are reviewed. Finally, potential future directions are discussed.
Keywords two-photon microscopy (TPM)      intravital imaging      pre-clinical tumor studies      cancer early detection      cancer diagnosis      medical imaging     
Corresponding Author(s): Jun LIU   
Online First Date: 16 April 2014    Issue Date: 24 June 2015
 Cite this article:   
Jun LIU. Two-photon microscopy in pre-clinical and clinical cancer research[J]. Front. Optoelectron., 2015, 8(2): 141-151.
 URL:  
https://academic.hep.com.cn/foe/EN/10.1007/s12200-014-0415-5
https://academic.hep.com.cn/foe/EN/Y2015/V8/I2/141
Fig.1  Jablonski diagram illustrating one- and two-photon excited fluorescence. Two-photon excited fluorescence results from the simultaneous absorption of two photons, each of half the energy of that from one-photon absorption
Fig.2  Gene expression and vasculature imaging in transgenic mice model by IV-TPM. EGFP was expressed upon aviation of VEGF. (a) and (b) TPM imaging at different depth of tumor, (a) 35–50 μm from the tumor surface and (b) 200 μm inside tumor, angiogenic blood vessels was observed with EGFP expressed host cells; (c) colocalization of VEGF-expressing host cells with angiogenic vessels; (d) single layer of (c) at twice magnification. Scale bars, 50 μm. Reprint from Ref. [49] with permission from publisher
Fig.3  Imaging motility of two cancer cell populations in mammary tumor with IV-TPM. (a) In vivo TPM imaging of tumor microenvironment. Macrophages (red), blood vessels (arrow), tumor cells (green and cyan), collagen (purple), labeled by Texas-Red, Dextran, GFP, intrinsic second?harmonic?generation (SHG) signal, respectively; (b) simultaneous imaging of motility of tumor cell of GFP or GFP/CFP expression induced by doxycycline; (c) cell motility with FP expression, induction of CFP expression did not affect cell motility. Scale bars, 100 μm. Reprint from Ref. [23] with permission from publisher
Fig.4  In vivo imaging of metabolism level of precancerous tissues by IV-TPM combined with FLIM at different depths. (a)–(c) Redox ratio, fluorescence intensity of FAD/NADH; (d)–(f) mean NADH lifetime; (g)–(i) mean FAD lifetime by FLIM imaging. High-grade precancer tissues (c), (f) and (i) were associated with high redox ratio, low NADH level and high FAD level compared to normal (a), (d) and (g) and low-grade precancer tissues (b), (e), and (h). Image size 100 μm × 100 μm. Reprint from Ref. [19] with permission from publisher
Fig.5  TPM images of malignant melanoma in human skin sample at upper epidermal (a), granular (b), spinous (c) and (d) layers. Four factors, epidermis disarray (a, highly fluorescent melanocytes, white arrows), poorly defined keratinocyte cell borders (b, c, d), pleomorphic and dendritic cells (c, d, asterisk, and arrows, respectively) were presented in human melanoma skin lesions. Scale bar, 40 μm. Reprint from Ref. [70] with permission from publisher
1 Yildiz A, Forkey J N, McKinney S A, Ha T, Goldman Y E, Selvin P R. Myosin V walks hand-over-hand: single fluorophore imaging with 1.5-nm localization. Science, 2003, 300(5628): 2061–2065
https://doi.org/10.1126/science.1084398 pmid: 12791999
2 Yildiz A, Park H, Safer D, Yang Z, Chen L Q, Selvin P R, Sweeney H L. Myosin VI steps via a hand-over-hand mechanism with its lever arm undergoing fluctuations when attached to actin. The Journal of Biological Chemistry, 2004, 279(36): 37223–37226
https://doi.org/10.1074/jbc.C400252200 pmid: 15254036
3 Myong S, Rasnik I, Joo C, Lohman T M, Ha T. Repetitive shuttling of a motor protein on DNA. Nature, 2005, 437(7063): 1321–1325
https://doi.org/10.1038/nature04049 pmid: 16251956
4 Tan E, Wilson T J, Nahas M K, Clegg R M, Lilley D M J, Ha T. A four-way junction accelerates hairpin ribozyme folding via a discrete intermediate. Proceedings of the National Academy of Sciences of the United States of America, 2003, 100(16): 9308–9313
https://doi.org/10.1073/pnas.1233536100 pmid: 12883002
5 Wang Y, Shyy J Y J, Chien S. Fluorescence proteins, live-cell imaging, and mechanobiology: seeing is believing. Annual Review of Biomedical Engineering, 2008, 10(1): 1–38
https://doi.org/10.1146/annurev.bioeng.010308.161731 pmid: 18647110
6 Perry S W, Burke R M, Brown E B. Two-photon and second harmonic microscopy in clinical and translational cancer research. Annals of Biomedical Engineering, 2012, 40(2): 277–291
https://doi.org/10.1007/s10439-012-0512-9 pmid: 22258888
7 Nguyen Q T, Olson E S, Aguilera T A, Jiang T, Scadeng M, Ellies L G, Tsien R Y. Surgery with molecular fluorescence imaging using activatable cell-penetrating peptides decreases residual cancer and improves survival. Proceedings of the National Academy of Sciences of the United States of America, 2010, 107(9): 4317–4322
https://doi.org/10.1073/pnas.0910261107 pmid: 20160097
8 Denk W, Strickler J H, Webb W W. Two-photon laser scanning fluorescence microscopy. Science, 1990, 248(4951): 73–76
https://doi.org/10.1126/science.2321027 pmid: 2321027
9 Fang H, Declerck Y A. Targeting the tumor microenvironment: from understanding pathways to effective clinical trials. Cancer Research, 2013, 73(16): 4965–4977
https://doi.org/10.1158/0008-5472.CAN-13-0661 pmid: 23913938
10 Cukierman E, Pankov R, Stevens D R, Yamada K M. Taking cell-matrix adhesions to the third dimension. Science, 2001, 294(5547): 1708–1712
https://doi.org/10.1126/science.1064829 pmid: 11721053
11 Swartz M A, Iida N, Roberts E W, Sangaletti S, Wong M H, Yull F E, Coussens L M, DeClerck Y A. Tumor microenvironment complexity: emerging roles in cancer therapy. Cancer Research, 2012, 72(10): 2473–2480
https://doi.org/10.1158/0008-5472.CAN-12-0122 pmid: 22414581
12 Fischbach C, Chen R, Matsumoto T, Schmelzle T, Brugge J S, Polverini P J, Mooney D J. Engineering tumors with 3D scaffolds. Nature Methods, 2007, 4(10): 855–860
https://doi.org/10.1038/nmeth1085 pmid: 17767164
13 Kenny P A, Lee G Y, Myers C A, Neve R M, Semeiks J R, Spellman P T, Lorenz K, Lee E H, Barcellos-Hoff M H, Petersen O W, Gray J W, Bissell M J. The morphologies of breast cancer cell lines in three-dimensional assays correlate with their profiles of gene expression. Molecular Oncology, 2007, 1(1): 84–96
https://doi.org/10.1016/j.molonc.2007.02.004 pmid: 18516279
14 Wang F, Weaver V M, Petersen O W, Larabell C A, Dedhar S, Briand P, Lupu R, Bissell M J. Reciprocal interactions between beta1-integrin and epidermal growth factor receptor in three-dimensional basement membrane breast cultures: a different perspective in epithelial biology. Proceedings of the National Academy of Sciences of the United States of America, 1998, 95(25): 14821–14826
https://doi.org/10.1073/pnas.95.25.14821 pmid: 9843973
15 Hosseinkhani H, Hosseinkhani M, Tian F, Kobayashi H, Tabata Y. Osteogenic differentiation of mesenchymal stem cells in self-assembled peptide-amphiphile nanofibers. Biomaterials, 2006, 27(22): 4079–4086
https://doi.org/10.1016/j.biomaterials.2006.03.030 pmid: 16600365
16 Jain R K, Duda D G, Clark J W, Loeffler J S. Lessons from phase III clinical trials on anti-VEGF therapy for cancer. Nature Clinical Practice Oncology, 2006, 3(1): 24–40
https://doi.org/10.1038/ncponc0403 pmid: 16407877
17 Benninger R K P, Hao M, Piston D W. Multi-photon excitation imaging of dynamic processes in living cells and tissues. In: Amara S G, Fleischmann B, Hebert S C, Lederer W J, Miyajima A, Zechner R, eds. Reviews of Physiology, Biochemistry and Pharmacology, 2008, 160: 71–92
https://doi.org/10.1007/112_2008_801
18 Helmchen F, Denk W. Deep tissue two-photon microscopy. Nature Methods, 2005, 2(12): 932–940
https://doi.org/10.1038/nmeth818 pmid: 16299478
19 Skala M C, Riching K M, Gendron-Fitzpatrick A, Eickhoff J, Eliceiri K W, White J G, Ramanujam N. In vivo multiphoton microscopy of NADH and FAD redox states, fluorescence lifetimes, and cellular morphology in precancerous epithelia. Proceedings of the National Academy of Sciences of the United States of America, 2007, 104(49): 19494–19499
https://doi.org/10.1073/pnas.0708425104 pmid: 18042710
20 Walsh A J, Cook R S, Manning H C, Hicks D J, Lafontant A, Arteaga C L, Skala M C. Optical metabolic imaging identifies glycolytic levels, subtypes, and early-treatment response in breast cancer. Cancer Research, 2013, 73(20): 6164–6174
https://doi.org/10.1158/0008-5472.CAN-13-0527 pmid: 24130112
21 Lim C S, Cho B R. Two-photon probes for biomedical applications. BMB Reports, 2013, 46(4): 188–194
https://doi.org/10.5483/BMBRep.2013.46.4.045 pmid: 23615259
22 Chudakov D M, Matz M V, Lukyanov S, Lukyanov K A. Fluorescent proteins and their applications in imaging living cells and tissues. Physiological Reviews, 2010, 90(3): 1103–1163
https://doi.org/10.1152/physrev.00038.2009 pmid: 20664080
23 Le Dévédec S E, Lalai R, Pont C, de Bont H, van de Water B. Two-photon intravital multicolor imaging combined with inducible gene expression to distinguish metastatic behavior of breast cancer cells in vivo. Molecular Imaging and Biology, 2011, 13(1): 67–77
24 Mahou P, Zimmerley M, Loulier K, Matho K S, Labroille G, Morin X, Supatto W, Livet J, Débarre D, Beaurepaire E. Multicolor two-photon tissue imaging by wavelength mixing. Nature Methods, 2012, 9(8): 815–818
https://doi.org/10.1038/nmeth.2098 pmid: 22772730
25 Shcherbo D, Merzlyak E M, Chepurnykh T V, Fradkov A F, Ermakova G V, Solovieva E A, Lukyanov K A, Bogdanova E A, Zaraisky A G, Lukyanov S, Chudakov D M. Bright far-red fluorescent protein for whole-body imaging. Nature Methods, 2007, 4(9): 741–746
https://doi.org/10.1038/nmeth1083 pmid: 17721542
26 Shcherbo D, Murphy C S, Ermakova G V, Solovieva E A, Chepurnykh T V, Shcheglov A S, Verkhusha V V, Pletnev V Z, Hazelwood K L, Roche P M, Lukyanov S, Zaraisky A G, Davidson M W, Chudakov D M. Far-red fluorescent tags for protein imaging in living tissues. The Biochemical Journal, 2009, 418(3): 567–574
https://doi.org/10.1042/BJ20081949 pmid: 19143658
27 Giepmans B N G, Adams S R, Ellisman M H, Tsien R Y. The fluorescent toolbox for assessing protein location and function. Science, 2006, 312(5771): 217–224
https://doi.org/10.1126/science.1124618 pmid: 16614209
28 Cahalan M D, Parker I, Wei S H, Miller M J. Two-photon tissue imaging: seeing the immune system in a fresh light. Nature Reviews. Immunology, 2002, 2(11): 872–880
https://doi.org/10.1038/nri935 pmid: 12415310
29 Toubai T, Sun Y, Luker G, Liu J, Luker K E, Tawara I, Evers R, Liu C, Mathewson N, Malter C, Nieves E, Choi S, Murphy K M, Reddy P. Host-derived CD8+ dendritic cells are required for induction of optimal graft-versus-tumor responses after experimental allogeneic bone marrow transplantation. Blood, 2013, 121(20): 4231–4241
https://doi.org/10.1182/blood-2012-05-432872 pmid: 23520337
30 Bestvater F, Spiess E, Stobrawa G, Hacker M, Feurer T, Porwol T, Berchner-Pfannschmidt U, Wotzlaw C, Acker H. Two-photon fluorescence absorption and emission spectra of dyes relevant for cell imaging. Journal of Microscopy, 2002, 208(Pt 2): 108–115
https://doi.org/10.1046/j.1365-2818.2002.01074.x pmid: 12423261
31 Liu B, Hu X L, Liu J, Zhao Y D, Huang Z L. Synthesis and photophysical properties of novel pyrimidine-based two-photon absorption chromophores. Tetrahedron Letters, 2007, 48(34): 5958–5962
https://doi.org/10.1016/j.tetlet.2007.06.122
32 Liu J, Chu J, Zhu H, Xu L, Zhang Z, Zeng S, Huang Z. A feasible method for comparing the power dependent photostability of fluorescent proteins. Chinese Optics Letters, 2008, 6(12): 941–943
https://doi.org/10.3788/COL20080612.0941
33 Liu J, Pei Z, Wang L, Zhang Z, Zeng S, Huang Z L. A straightforward and quantitative approach for characterizing the photoactivation performance of optical highlighter fluorescent proteins. Applied Physics Letters, 2010, 97(20): 203701
https://doi.org/10.1063/1.3518471
34 Zou L, Liu Z, Yan X, Liu Y, Fu Y, Liu J, Huang Z, Chen X, Qin J. Star-shaped D-pi-A molecules containing a 2,4,6-Tri(thiophen-2-yl)-1,3,5-triazine unit: synthesis and two-photon absorption properties. European Journal of Organic Chemistry, 2009, 2009(32): 5587–5593
https://doi.org/10.1002/ejoc.200900641
35 Wagner R. Erl?uterungstaflen zur Physiologie und Entwicklungsgeschichte. Germany, Leipzig: Leopold Voss, 1839
36 Wood S Jr. Pathogenesis of metastasis formation observed in vivo in the rabbit ear chamber. AMA Archives of Pathology, 1958, 66(4): 550–568
pmid: 13582395
37 Chishima T, Miyagi Y, Wang X, Yamaoka H, Shimada H, Moossa A R, Hoffman R M. Cancer invasion and micrometastasis visualized in live tissue by green fluorescent protein expression. Cancer Research, 1997, 57(10): 2042–2047
pmid: 9158003
38 Farina K L, Wyckoff J B, Rivera J, Lee H, Segall J E, Condeelis J S, Jones J G. Cell motility of tumor cells visualized in living intact primary tumors using green fluorescent protein. Cancer Research, 1998, 58(12): 2528–2532
pmid: 9635573
39 MacDonald I C, Schmidt E E, Morris V L, Chambers A F, Groom A C. Intravital videomicroscopy of the chorioallantoic microcirculation: a model system for studying metastasis. Microvascular Research, 1992, 44(2): 185–199
https://doi.org/10.1016/0026-2862(92)90079-5 pmid: 1474926
40 Araya R, Eisenthal K B, Yuste R. Dendritic spines linearize the summation of excitatory potentials. Proceedings of the National Academy of Sciences of the United States of America, 2006, 103(49): 18799–18804
https://doi.org/10.1073/pnas.0609225103 pmid: 17132736
41 Araya R, Jiang J, Eisenthal K B, Yuste R. The spine neck filters membrane potentials. Proceedings of the National Academy of Sciences of the United States of America, 2006, 103(47): 17961–17966
https://doi.org/10.1073/pnas.0608755103 pmid: 17093040
42 Ngo-Anh T J, Bloodgood B L, Lin M, Sabatini B L, Maylie J, Adelman J P. SK channels and NMDA receptors form a Ca2+-mediated feedback loop in dendritic spines. Nature Neuroscience, 2005, 8(5): 642–649
https://doi.org/10.1038/nn1449 pmid: 15852011
43 Matsumoto-Ida M, Akao M, Takeda T, Kato M, Kita T. Real-time 2-photon imaging of mitochondrial function in perfused rat hearts subjected to ischemia/reperfusion. Circulation, 2006, 114(14): 1497–1503
https://doi.org/10.1161/CIRCULATIONAHA.106.628834 pmid: 17000908
44 Gupta A, Rhodes G J, Berg D T, Gerlitz B, Molitoris B A, Grinnell B W. Activated protein C ameliorates LPS-induced acute kidney injury and downregulates renal INOS and angiotensin 2. American Journal of Physiology, Renal Physiology, 2007, 293(1): F245–F254
https://doi.org/10.1152/ajprenal.00477.2006 pmid: 17409278
45 Nishimura N, Schaffer C B, Friedman B, Lyden P D, Kleinfeld D. Penetrating arterioles are a bottleneck in the perfusion of neocortex. Proceedings of the National Academy of Sciences of the United States of America, 2007, 104(1): 365–370
https://doi.org/10.1073/pnas.0609551104 pmid: 17190804
46 Schwickert T A, Lindquist R L, Shakhar G, Livshits G, Skokos D, Kosco-Vilbois M H, Dustin M L, Nussenzweig M C. In vivo imaging of germinal centres reveals a dynamic open structure. Nature, 2007, 446(7131): 83–87
https://doi.org/10.1038/nature05573 pmid: 17268470
47 Boissonnas A, Fetler L, Zeelenberg I S, Hugues S, Amigorena S. In vivo imaging of cytotoxic T cell infiltration and elimination of a solid tumor. The Journal of Experimental Medicine, 2007, 204(2): 345–356
https://doi.org/10.1084/jem.20061890 pmid: 17261634
48 Jain R K. Determinants of tumor blood flow: a review. Cancer Research, 1988, 48(10): 2641–2658
pmid: 3282647
49 Brown E B, Campbell R B, Tsuzuki Y, Xu L, Carmeliet P, Fukumura D, Jain R K. In vivo measurement of gene expression, angiogenesis and physiological function in tumors using multiphoton laser scanning microscopy. Nature Medicine, 2001, 7(7): 864–868
https://doi.org/10.1038/89997 pmid: 11433354
50 Stroh M, Zimmer J P, Duda D G, Levchenko T S, Cohen K S, Brown E B, Scadden D T, Torchilin V P, Bawendi M G, Fukumura D, Jain R K. Quantum dots spectrally distinguish multiple species within the tumor milieu in vivo. Nature Medicine, 2005, 11(6): 678–682
https://doi.org/10.1038/nm1247 pmid: 15880117
51 Wang W, Wyckoff J B, Frohlich V C, Oleynikov Y, Hüttelmaier S, Zavadil J, Cermak L, Bottinger E P, Singer R H, White J G, Segall J E, Condeelis J S. Single cell behavior in metastatic primary mammary tumors correlated with gene expression patterns revealed by molecular profiling. Cancer Research, 2002, 62(21): 6278–6288
pmid: 12414658
52 Sahai E, Wyckoff J, Philippar U, Segall J E, Gertler F, Condeelis J. Simultaneous imaging of GFP, CFP and collagen in tumors in vivo using multiphoton microscopy. BMC Biotechnology, 2005, 5(1): 14
https://doi.org/10.1186/1472-6750-5-14 pmid: 15910685
53 Condeelis J, Segall J E. Intravital imaging of cell movement in tumours. Nature Reviews. Cancer, 2003, 3(12): 921–930
https://doi.org/10.1038/nrc1231 pmid: 14737122
54 Wang W, Wyckoff J B, Goswami S, Wang Y, Sidani M, Segall J E, Condeelis J S. Coordinated regulation of pathways for enhanced cell motility and chemotaxis is conserved in rat and mouse mammary tumors. Cancer Research, 2007, 67(8): 3505–3511
https://doi.org/10.1158/0008-5472.CAN-06-3714 pmid: 17440055
55 Wolf K, Mazo I, Leung H, Engelke K, von Andrian U H, Deryugina E I, Strongin A Y, Br?cker E B, Friedl P. Compensation mechanism in tumor cell migration: mesenchymal-amoeboid transition after blocking of pericellular proteolysis. The Journal of Cell Biology, 2003, 160(2): 267–277
https://doi.org/10.1083/jcb.200209006 pmid: 12527751
56 Wyckoff J B, Jones J G, Condeelis J S, Segall J E. A critical step in metastasis: in vivo analysis of intravasation at the primary tumor. Cancer Research, 2000, 60(9): 2504–2511
pmid: 10811132
57 Wyckoff J B, Pinner S E, Gschmeissner S, Condeelis J S, Sahai E. ROCK- and myosin-dependent matrix deformation enables protease-independent tumor-cell invasion in vivo. Current Biology: CB, 2006, 16(15): 1515–1523
https://doi.org/10.1016/j.cub.2006.05.065 pmid: 16890527
58 Wyckoff J B, Wang Y, Lin E Y, Li J F, Goswami S, Stanley E R, Segall J E, Pollard J W, Condeelis J. Direct visualization of macrophage-assisted tumor cell intravasation in mammary tumors. Cancer Research, 2007, 67(6): 2649–2656
https://doi.org/10.1158/0008-5472.CAN-06-1823 pmid: 17363585
59 Warburg O. On the origin of cancer cells. Science, 1956, 123(3191): 309–314
https://doi.org/10.1126/science.123.3191.309 pmid: 13298683
60 Zhang Q, Piston D W, Goodman R H. Regulation of corepressor function by nuclear NADH. Science, 2002, 295(5561): 1895–1897
pmid: 11847309
61 Zhang Q, Wang S Y, Nottke A C, Rocheleau J V, Piston D W, Goodman R H. Redox sensor CtBP mediates hypoxia-induced tumor cell migration. Proceedings of the National Academy of Sciences of the United States of America, 2006, 103(24): 9029–9033
https://doi.org/10.1073/pnas.0603269103 pmid: 16740659
62 Heart E, Yaney G C, Corkey R F, Schultz V, Luc E, Liu L, Deeney J T, Shirihai O, Tornheim K, Smith P J S, Corkey B E. Ca2+, NAD(P)H and membrane potential changes in pancreatic beta-cells by methyl succinate: comparison with glucose. The Biochemical Journal, 2007, 403(1): 197–205
https://doi.org/10.1042/BJ20061209 pmid: 17181533
63 Jung J C, Schnitzer M J. Multiphoton endoscopy. Optics Letters, 2003, 28(11): 902–904
https://doi.org/10.1364/OL.28.000902 pmid: 12816240
64 Kim P, Puoris’haag M, C?té D, Lin C P, Yun S H. In vivo confocal and multiphoton microendoscopy. Journal of Biomedical Optics, 2008, 13(1): 010501
https://doi.org/10.1117/1.2839043 pmid: 18315346
65 Koehler M J, Speicher M, Lange-Asschenfeldt S, Stockfleth E, Metz S, Elsner P, Kaatz M, K?nig K. Clinical application of multiphoton tomography in combination with confocal laser scanning microscopy for in vivo evaluation of skin diseases. Experimental Dermatology, 2011, 20(7): 589–594
https://doi.org/10.1111/j.1600-0625.2011.01279.x pmid: 21539618
66 Meyer T, Bergner N, Bielecki C, Krafft C, Akimov D, Romeike B F M, Reichart R, Kalff R, Dietzek B, Popp J. Nonlinear microscopy, infrared, and Raman microspectroscopy for brain tumor analysis. Journal of Biomedical Optics, 2011, 16(2): 021113-1–021113-3
https://doi.org/10.1117/1.3533268
67 Breunig H G, Studier H, K?nig K. Multiphoton excitation characteristics of cellular fluorophores of human skin in vivo. Optics Express, 2010, 18(8): 7857–7871
https://doi.org/10.1364/OE.18.007857 pmid: 20588627
68 Chen J, Lee A, Zhao J, Wang H, Lui H, McLean D I, Zeng H. Spectroscopic characterization and microscopic imaging of extracted and in situ cutaneous collagen and elastic tissue components under two-photon excitation. Skin Research and Technology, 2009, 15(4): 418–426
https://doi.org/10.1111/j.1600-0846.2009.00381.x pmid: 19832952
69 Paoli J, Smedh M, Ericson M B. Multiphoton laser scanning microscopy—a novel diagnostic method for superficial skin cancers. Seminars in Cutaneous Medicine and Surgery, 2009, 28(3): 190–195
https://doi.org/10.1016/j.sder.2009.06.007 pmid: 19782943
70 Dimitrow E, Ziemer M, Koehler M J, Norgauer J, K?nig K, Elsner P, Kaatz M. Sensitivity and specificity of multiphoton laser tomography for in vivo and ex vivo diagnosis of malignant melanoma. The Journal of Investigative Dermatology, 2009, 129(7): 1752–1758
https://doi.org/10.1038/jid.2008.439 pmid: 19177136
71 Piletic I R, Matthews T E, Warren W S. Probing near-infrared photorelaxation pathways in eumelanins and pheomelanins. The Journal of Physical Chemistry A, 2010, 114(43): 11483–11491
https://doi.org/10.1021/jp103608d pmid: 20882951
72 Matthews T E, Piletic I R, Selim M A, Simpson M J, Warren W S. Pump-probe imaging differentiates melanoma from melanocytic nevi. Science Translational Medicine, 2011, 3(71): 71ra15
https://doi.org/10.1126/scitranslmed.3001604 pmid: 21346168
73 Matthews T E, Wilson J W, Degan S, Simpson M J, Jin J Y, Zhang J Y, Warren W S. In vivo and ex vivo epi-mode pump-probe imaging of melanin and microvasculature. Biomedical Optics Express, 2011, 2(6): 1576–1583
https://doi.org/10.1364/BOE.2.001576 pmid: 21698020
74 Gu M, Bao H C, Li J L. Cancer-cell microsurgery using nonlinear optical endomicroscopy. Journal of Biomedical Optics, 2010, 15(5): 050502
https://doi.org/10.1117/1.3502566 pmid: 21054074
75 Li D, Zeng S, Lv X, Liu J, Du R, Jiang R, Chen W R, Luo Q. Dispersion characteristics of acousto-optic deflector for scanning Gaussian laser beam of femtosecond pulses. Optics Express, 2007, 15(8): 4726–4734
https://doi.org/10.1364/OE.15.004726 pmid: 19532718
76 Zeng S, Li D, Lv X, Liu J, Luo Q. Pulse broadening of the femtosecond pulses in a Gaussian beam passing an angular disperser. Optics Letters, 2007, 32(9): 1180–1182
https://doi.org/10.1364/OL.32.001180 pmid: 17410275
77 Flusberg B A, Cocker E D, Piyawattanametha W, Jung J C, Cheung E L M, Schnitzer M J. Fiber-optic fluorescence imaging. Nature Methods, 2005, 2(12): 941–950
https://doi.org/10.1038/nmeth820 pmid: 16299479
78 Fu L, Gu M. Fibre-optic nonlinear optical microscopy and endoscopy. Journal of Microscopy, 2007, 226(Pt 3): 195–206
https://doi.org/10.1111/j.1365-2818.2007.01777.x pmid: 17535259
79 Le Harzic R, Riemann I, Weinigel M, K?nig K, Messerschmidt B. Rigid and high-numerical-aperture two-photon fluorescence endoscope. Applied Optics, 2009, 48(18): 3396–3400
https://doi.org/10.1364/AO.48.003396 pmid: 19543347
80 Lelek M, Suran E, Louradour F, Barthelemy A, Viellerobe B, Lacombe F. Coherent femtosecond pulse shaping for the optimization of a non-linear micro-endoscope. Optics Express, 2007, 15(16): 10154–10162
https://doi.org/10.1364/OE.15.010154 pmid: 19547364
81 Meier R, Kromer K, Stepp H, Sroka R. A comparison of confocal and two-photon microendoscopy. In: Dossel O, Schlegel W C, eds. World Congress on Medical Physics and Biomedical Engineering, 2009, 25(6): 177–178
82 Llewellyn M E, Barretto R P J, Delp S L, Schnitzer M J. Minimally invasive high-speed imaging of sarcomere contractile dynamics in mice and humans. Nature, 2008, 454(7205): 784–788
pmid: 18600262
83 Paull P E, Hyatt B J, Wassef W, Fischer A H. Confocal laser endomicroscopy: a primer for pathologists. Archives of Pathology & Laboratory Medicine, 2011, 135(10): 1343–1348
https://doi.org/10.5858/arpa.2010-0264-RA pmid: 21970490
84 Gulsen G, Yu H, Wang J, Nalcioglu O, Merritt S, Bevilacqua F, Durkin A J, Cuccia D J, Lanning R, Tromberg B J. Congruent MRI and near-infrared spectroscopy for functional and structural imaging of tumors. Technology in Cancer Research & Treatment, 2002, 1(6): 497–505
pmid: 12625777
85 Ntziachristos V, Yodh A G, Schnall M D, Chance B. MRI-guided diffuse optical spectroscopy of malignant and benign breast lesions. Neoplasia (New York, N.Y.), 2002, 4(4): 347–354
https://doi.org/10.1038/sj.neo.7900244 pmid: 12082551
86 Zhu Q, Tannenbaum S, Kurtzman S H. Optical tomography with ultrasound localization for breast cancer diagnosis and treatment monitoring. Surgical Oncology Clinics of North America, 2007, 16(2): 307–321
https://doi.org/10.1016/j.soc.2007.03.008 pmid: 17560514
87 Zhu Q, Kurtzma S H, Hegde P, Tannenbaum S, Kane M, Huang M, Chen N G, Jagjivan B, Zarfos K. Utilizing optical tomography with ultrasound localization to image heterogeneous hemoglobin distribution in large breast cancers. Neoplasia (New York, N.Y.), 2005, 7(3): 263–270
https://doi.org/10.1593/neo.04526 pmid: 15799826
88 McCann C M, Waterman P, Figueiredo J L, Aikawa E, Weissleder R, Chen J W. Combined magnetic resonance and fluorescence imaging of the living mouse brain reveals glioma response to chemotherapy. NeuroImage, 2009, 45(2): 360–369
https://doi.org/10.1016/j.neuroimage.2008.12.022 pmid: 19154791
[1] Jacqueline GUNTHER, Stefan ANDERSSON-ENGELS. Review of current methods of acousto-optical tomography for biomedical applications[J]. Front. Optoelectron., 2017, 10(3): 211-238.
[2] Zhen WANG. Recent advances of optical imaging in animal stroke model[J]. Front Optoelec, 2013, 6(2): 134-145.
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