Pulse-modulated second harmonic imaging microscope quantitatively demonstrates marked increase of collagen in tumor after chemotherapy

Journal of Biomedical Optics

Volumn 15, Issue 5, 2010, Pages

  Raja, Anju M ^a,b,c   Xu, Shuoyu ^a,d   Sun, Wanxin ^a   Zhou, Jianbiao ^b,d   Tai, Dean C S ^d   Chen, Chien Shing ^c,e   Rajapakse, Jagath C ^d,f   So, Peter T C ^d,g,h   Yu, Hanry ^a,b,d,f  

^a INSTITUTE OF BIOENGINEERING AND NANOTECHNOLOGY   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c NATIONAL UNIVERSITY HEALTH SYSTEM   (Singapore)

^d SINGAPORE MIT ALLIANCE   (Singapore)

^e LOMA LINDA UNIVERSITY   (United States)

^f NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^g SINGAPORE MIT ALLIANCE FOR RESEARCH AND TECHNOLOGY   (Singapore)

^h Massachusetts Institute of Technology Cambridge   (United States)

Author keywords

collagen modulation postchemotherapy; drug resistance; pulse modulation; second harmonic generation imaging

Indexed keywords

ACUTE MYELOID LEUKEMIA; COLLAGEN FIBER; DRUG RESISTANCE; RECEPTOR TYROSINE KINASE; SECOND HARMONIC GENERATION; SECOND-HARMONIC IMAGING; SPATIAL DISTRIBUTION; TUMOR RESPONSE;

AMINO ACIDS; CHEMOTHERAPY; COLLAGEN; HARMONIC ANALYSIS; NONLINEAR OPTICS; PULSE MODULATION; SIGNAL TO NOISE RATIO; TUMORS;

HARMONIC GENERATION;

ANTINEOPLASTIC AGENT; CARBANILAMIDE DERIVATIVE; COLLAGEN; DIAGNOSTIC AGENT; INDAZOLE DERIVATIVE; N (4 (3 AMINO 1H INDAZOL 4 YL)PHENYL) N1 (2 FLUORO 5 METHYLPHENYL)UREA; N-(4-(3-AMINO-1H-INDAZOL-4-YL)PHENYL)-N1-(2-FLUORO-5-METHYLPHENYL)UREA; PROTEIN TYROSINE KINASE;

ACUTE GRANULOCYTIC LEUKEMIA; ANIMAL; ARTICLE; COMPUTER ASSISTED DIAGNOSIS; DRUG ANTAGONISM; EVALUATION; FEMALE; HUMAN; INSTRUMENTATION; LASER; LIGHT RELATED PHENOMENA; METABOLISM; METHODOLOGY; MICROSCOPY; MOUSE; MOUSE MUTANT; NEOPLASM; PATHOLOGY; TUMOR CELL LINE; XENOGRAFT;

ANIMALS; ANTINEOPLASTIC AGENTS; CELL LINE, TUMOR; COLLAGEN; FEMALE; HUMANS; IMAGE INTERPRETATION, COMPUTER-ASSISTED; INDAZOLES; LASERS; LEUKEMIA, MYELOID, ACUTE; MICE; MICE, SCID; MICROSCOPY; NEOPLASMS; OPTICAL PHENOMENA; PHENYLUREA COMPOUNDS; RECEPTOR PROTEIN-TYROSINE KINASES; TRANSPLANTATION, HETEROLOGOUS;

EID: 78149424629     PISSN: 10833668     EISSN: 15602281     Source Type: Journal    
DOI: 10.1117/1.3497565     Document Type: Article

References (54)

1. J. Zhou et al., "Synergistic antileukemic effects between ABT-869 and chemotherapy involve downregulation of cell cycle-regulated genes and c-Mos-mediated MAPK pathway," Leukemia 22(1), 138-146 (2008).
2. H. F. Dvorak, J. Flier, and H. Frank, "Tumors wounds that do not heal similarities between tumor stroma generation and wound healing," N. Engl. J. Med. 315(26), 1650-1659 (1986).
3. J. Hay, S. Shahzeidi, and G. Laurent, "Mechanisms of Bleomycin-induced lung damage," Arch. Toxicol. 65(2), 81-94 (1991).
4. H. Tsuchiya, Y. Ueda, K. Tomita, I. Nakanishi, and A. Roessner, "Chemotherapeutci effect on osteosarcoma on basis of collagen analysis a proposal of the induction of osteosarcoma differentiation," J. Cancer Res. Clin. Oncol. 119(12), 702-706 (1993).
5. R. K. Jain, D. G. Duda, C. G. Willett, D. V. Sahani, A. X. Zhu, J. S. Loeffler, T. T. Batchelor, and A. G. Sorensen, "Biomarkers of response and resistance to antiangiogenic therapy," Nature Rev. Clin. Oncol. 6(6), 327-338 (2009).
6. P. J. Campagnola, A. C. Millard, M. Terasaki, P. E. Hoppe, C. J. Malone, and W. A. Mohler, "Three-dimensional high-resolution second-harmonic generation imaging of endogenous structural proteins in biological tissues," Biophys. J. 82(1), 493-508 (2002).
7. R. M. Williams, D. W. Piston, and W. W. Webb, "2-photon molecular excitation provides intrinsic 3-dimensional resolution for laser-based microscopy and microphotochemistry," FASEB J. 8(11), 804-813 (1994).
8. S. J. Lin, J. S. Kuo, C. J. Wu, R. J. Lin, W C. Chen, J. S. Liao, Y. H. Hsu, C. J. Tsai, T. F. Chen, and D. C. Yu, "Discrimination of basal cell carcinoma from normal dermal stroma by quantitative multipho-ton imaging," Opt. Lett. 31(18), 2756-2758 (2006).
9. P. Wilder-Smith, W G. Jung, J. Zhang, Z. Chen, K. Osann, and B. Tromberg, "Noninvasive imaging of oral premalignancy and malignancy," J. Biomed. Opt. 10(5), 051601 (2005).
10. P. J. Campagnola, M.-d. WeiA. Lewisand L. M. Loew"High-resolution nonlinear optical imaging of live cells by second harmonic generation," Biophys. J. 77(6), 3341-3349 (1999).
11. J. G. Lyubovitsky, T. B. Krasieva, X. Xu, B. Andersen, and B. J. Tromberg, "In situ multiphoton optical tomography of hair follicles in mice," J. Biomed. Opt. 12(4), 044003 (2007).
12. D. W Piston, "Imaging living cells and tissues by two-photon excitation microscopy," Trends Cell Biol. 9(2), 66-69 (1999).
13. C. Soeller and M. B. Cannell, "Construction of a two-photon microscope and optimisation of illumination pulse duration," Pflugers Arch. Eur. J. Physiol. 432(3), 555-561 (1996).
14. T. Ragan, J. D. Sylvan, K. H. Kim, H. Huang, K. Bahlmann, R. T. Lee, and P. T. C. So, "High-resolution whole organ imaging using two-photon tissue cytometry," J. Biomed. Opt. 12(1), 014015 (2007).
15. Q. F Wu and A. T. Yeh, "Rabbit cornea microstructure response to changes intraocular pressure visualized by using nonlinear optical microscopy," Cornea 27(2), 202-208 (2008).
16. M. Strupler, A.-M. Pena, M. Hernest, P.-L. Tharaux, J.-L. Martin, E. Beaurepaire, and M.-C. Schanne-Klein, "Second harmonic imaging and scoring of collagen in fibrotic tissues," Opt. Express 15(7), 4054-4065 (2007).
17. N. D. Kirkpatrick, S. Andreou, J. B. Hoying, and U. Utzinger, "Live imaging of collagen remodeling during angiogenesis," Am. J. Physiol. Heart Circ. Physiol. 292(6), H3198-H3206 (2007).
18. M.-H. Chen, W.-L. Chen, Y. Sun, P. T. Fwu, and C.-Y Dong, "Multiphoton autofluorescence and second-harmonic generation imaging of the tooth," J. Biomed. Opt. 12(6), 064018 (2007).
19. P. P. Provenzano, C. T. Rueden, S. M. Trier, L. Yan, S. M. Ponik, D. R. Inman, P. J. Keely, and K. W Eliceiri, "Nonlinear optical imaging and spectral-lifetime computational analysis of endogenous and exogenous fluorophores in breast cancer," J. Biomed. Opt. 13(3), 031220 (2008).
20. P. P. Provenzano, K. W Elicein, L. Yan, A. Ada-Nguema, M. W Conklin, D. R. Inman, and P. J. Keely, "Nonlinear optical imaging of cellular processes in breast cancer," Microsc. Microanal. 14(6), 532-548 (2008).
21. S. M. Zhuo, J. X. Chen, T. S. Luo, X. S. Jiang, S. S. Xie, and R. Chen, "Two-layered multiphoton microscopic imaging of cervical tissue," Lasers Med. Sci. 24(3), 359-363 (2009).
22. P. P. Provenzano, K. W Eliceiri, J. M. Campbell, D. R. Inman, J. G. White, and P. J. Keely, "Collagen reorganization at the tumor-stromal interface facilitates local invasion," Bmc Med. 4 (2006).
23. N. D. Kirkpatrick, M. A. Brewer, and U. Utzinger, "Endogenous optical biomarkers of ovarian cancer evaluated with multiphoton microscopy," Cancer Epidemiol. Biomarkers Prev. 16(10), 2048-2057 (2007).
24. E. Brown, T. McKee, E. diTomaso, A. Pluen, B. Seed, Y. Boucher, and R. K. Jain, "Dynamic imaging of collagen and its modulation in tumors in vivo using second-harmonic generation," Nat. Med. 9(6), 796-800 (2003).
25. O. Chernyavskiy, L. Vannucci, P. Bianchini, F Difato, M. Saieh, and L. Kubínová, "Imaging of mouse experimental melanoma in vivo and ex vivo by combination of confocal and nonlinear microscopy," Microsc. Res. Tech. 72(6), 411-423 (2009).
26. X. Han, R. M. Burke, M. L. Zettel, P. Tang, and E. R. Brown, "Second harmonic properties of tumor collagen: determining the structural relationship between reactive stroma and healthy stroma," Opt. Express 16(3), 1846-1859 (2008).
27. P. P. Provenzano, K. W Eliceiri, and P. J. Keely, "Multiphoton microscopy and fluorescence lifetime imaging microscopy (FLIM) to monitor metastasis and the tumor microenvironment," Clin. Exp. Metastasis 26(4), 357-370 (2009).
28. C.-C. Wang, F.-C. Li, R.-J. Wu, V. A. Hovhannisyan, W.-C. Lin, S.-J. Lin, P. T. C. So, and C.-Y. Dong, "Differentiation of normal and cancerous lung tissues by multiphoton imaging," J. Biomed. Opt. 14(4), 044034 (2009).
29. S. M. Zhuo, J. Chen, S. Xie, Z. Hong, and X. Jiang, "Extracting diagnostic stromal organization features based on intrinsic two-photon excited fluorescence and second-harmonic generation signals," J. Biomed. Opt. 14(2), 020503 (2009).
30. R. M. Williams, A. Flesken-Nikitin, L. H. Ellenson, D. C. Connolly, T. C. Hamilton, A. Y. Nikitin, and W R. Zipfel, "Strategies for high-resolution imaging of epithelial ovarian cancer by laparoscopic nonlinear microscopy," Trans. Oncol. 3(3), 181-194 (2010).
31. T. Hompland, A. Erikson, M. Lindgren, T. Lindmo, and C. de Lande Davis, "Second-harmonic generation in collagen as a potential cancer diagnostic parameter," J. Biomed. Opt. 13(5), 054050 (2008).
32. M. Muller, J. Squier, R. Wolleschensky, U. Simon, and G. J. Brak-enhoff, "Dispersion pre-compensation of 15 femtosecond optical pulses for high-numerical-aperture objectives," J. Microscopy-Oxford 191, 141-150 (1998). (Pubitemid 28378439)
33. R. L. Fork, O. E. Martinez, and J. P. Gordon, "Negative dispersion using pair of prisms," Opt. Lett. 9(5), 150-152 (1984).
34. V. Iyer, B. E. Losavio, and P. Saggau, "Compensation of spatial and temporal dispersion for acousto-optic multiphoton laser-scanning microscopy," J. Biomed. Opt. 8(3), 460-471 (2003).
35. S. Tang, T. B. Krasieva, Z. Chen, G. Tempea, and B. J. Tromberg, "Effect of pulse duration on two-photon excited fluorescence and second harmonic generation in nonlinear optical microscopy," J. Biomed. Opt. 11(2), 020501 (2006).
36. L. T. Schelhas and M. Dantus, "Advantages of ultrashort phase-shaped pulses for selective two-photon activation and biomedical imaging," Nanomed. 2(3), 177-181 (2006).
37. S. Akturk, M. Kimmel, P. O'Shea, and R. Trebino, "Extremely simple device for measuring 20-fs pulses," Opt. Lett. 29(9), 1025-1027 (2004).
38. D. B. Shankar et al., "ABT-869, a multitargeted receptor tyrosine kinase inhibitor: inhibition of FLT3 phosphorylation and signaling in acute myeloid leukemia," Blood 109(8), 3400-3408 (2007).
39. A. P. Dempster, N. M. Laird, and D. B. Rubin, "Maximum likelihood from incomplete data via the EM algorithm," J. Royal Stat. Soc. Series B 39(1), 1-38 (1977).
40. A. M. Stein, D. A. Vader, L. M. Jawerth, D. A. Weitz, and L. M. Sander, "An algorithm for extracting the network geometry of 3d collagen gels," J. Microsc. 232(3), 961-968 (2008).
41. P. Bedossa et al., "Intraobserver and interobserver variations in liver-biopsy intepretation in patients with chronic hepatitis-C," Hepatol. 20(1), 15-20 (1994).
42. A. Theodossi et al., "Observer variation and discriminatory value of biopsy features in inflammatory bowel-disease," Gut 35(7), 961-968 (1994).
43. S. S. Baroni et al., "Stimulatory autoantibodies to the PDGF receptor in systemic sclerosis," N. Engl. J. Med. 354(25), 2667-2676 (2006).
44. H. Green, G. J. Todaro, and B. Goldberg, "Collagen synthesis in fibroblasts transformed by oncogenic viruses," Nature 209(5026), 916 (1966).
45. J. Smolle, M. Fiebiger, R. Hofmann-Wellenhof, and H. Kerl, "Quantitative morphology of collagen fibers in cutaneous malignant melanoma and melanocytic nevus," Am. J. Dermatopathol. 18(4), 358-363 (1996).
46. B. R. Lester and J. B. McCarthy, "Tumor-cell adhesion to the extracellular-matrix and signal transduction mechanisms implicated in tumor-cell motility, invasion and metastasis," Cancer Metastasis Rev. 11(1), 31-44 (1992).
47. S. Misra, S. Ghatak, and B. P. Toole, "Regulation of MDR1 expression and drug resistance by a positive feedback loop involving hy-aluronan, phosphoinositide 3-kinase, and ErbB2," J. Biolog. Chem. 280(21), 20310-20315 (2005).
48. V. M. Weaver, S. Lelièvre, J. N. Lakins, M. A. Chrenek, J. C. R. Jones, F. Giancotti, Z. Werb, M. J. Bissell, Beta 4 integrin-dependent formation of polarized three-dimensional architecture confers resistance to apoptosis in normal and malignant mammary epithelium, Cancer Cells 2, 3, 205-216 (2002)
49. L. A. Hazlehurst, N. Valkov, L. Wisner, J. A. Storey, D. Boulware, D. M. Sullivan, and W. S. Dalton, "Reduction in drug-induced DNA double-strand breaks associated with beta 1 integrin-mediated adhesion correlates with drug resistance in U937 cells," Blood 98(6), 1897-1903 (2001).
50. P. Farmer et al., "A stroma-related gene signature predicts resistance to neoadjuvant chemotherapy in breast cancer," Nat. Med. 15(2), 220-220 (2009).
51. M. J. Newman, "Transforming growth-factor-Beta and the cell surface in tumor progression," Cancer Metastasis Rev. 12(3-4), 239-254 (1993).
52. O. Purps, B. Lahme, A. M. Gressner, N. M. Meindi-Beinker, and S. Dooley, "Loss of TGF-beta dependent growth control during HSC transdifferentiation, " Biochem. Biophys. Res. Commun. 353(3), 841-847 (2007).
53. P. P. Provenzano, D. R. Inman, K. W. Eliceiri, and P. J. Keely, "Matrix density-induced mechanoregulation of breast cell phenotype, signaling and gene expression through a FAK-ERK linkage," Oncogene 28(49), 4326-4343 (2009).
54. G. Ranieri and G. Gasparini, "Angiogenesis and angiogenesis inhibitors: a new potential anticancer therapeutic strategy," Curr. Drug Targets Immune, Endocrine Metabolic Disorders 1(3), 241-53 (2001).