Abstract

Oocyte and embryo selection governs the success of assisted reproductive technologies. The imaging tools applied for selecting embryos may need to contain several key properties: noninvasiveness, high 3D resolution, and the contrast capability to provide as much information about the embryos as possible, such as spindle fibers, zona pellucida, and organelles. Currently adopted imaging techniques can only provide one or two of these desired properties and are with limited contrast of the embryos. Some image techniques can even damage the embryos. Previous studies have shown that harmonic generation microscopy (HGM), a virtual-transition based technology, can provide noninvasive imaging in zebrafish embryos with a sub-cellular 3D resolution and a millimeter penetration depth, and thus could be a suitable tool for future oocyte and embryo selection of assisted reproductive technologies. However to evaluate HGM in clinical use, the intrinsic contrast origin of the second harmonic generation (SHG) and third harmonic generation (THG) inside the mammal embryos has to be studied. In this work we performed HGM studies on the in vitro cultured mouse oocytes and embryos by combining the SHG and THG modalities, with a focus on the contrast origin evaluation. Through the noninvasive HGM imaging, we can clearly identify various structures in the whole oocytes and embryos, including spindle fibers, zona pellucida, polar bodies, cell membranes, and the laminated organelles in the cells. The origin of the THG contrast was further confirmed through the standard staining studies. Through SHG signals, we could not only observe the spindle fibers when the oocytes were arrested at metaphase II or during the cleavage of the embryos, but can also distinguish and analyze the thickness of the three layers of the zona pellucida. Combining two different higher-harmonic generation modalities, SHG and THG, HGM successfully revealed the subcellular structures of the whole mouse embryos with a high 3D spatial resolution.

© 2008 Optical Society of America

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2008 (1)

C.-H. Yu, S.-P. Tai, C.-T. Kung, W.-J. Lee, Y.-F. Chan, H.-L. Liu, J.-Y. Lyu, and C.-K. Sun, “Molecular thirdharmonic- generation microscopy through resonance enhancement with absorbing dye,” Opt. Lett 33, 387–389 (2008).
[Crossref] [PubMed]

2007 (4)

M. Shribak, J. LaFountain, D. Biggs, and S. Inouè, “Quantitative orientation-independent differential interference contrast (DIC) microscopy coupled with orientation-independent polarization microscopy,” Microsc. Microanal 13, 10–11 (2007).
[PubMed]

J. Holte, L. Berglund, K. Milton, C. Garello, G. Gennarelli, A. Revelli, and T. Bergh “Construction of an evidence-based integrated morphology cleavage embryo score for implantation potential of embryos scored and transferred on day 2 after oocyte retrieval,” Hum. Reprod 22, 548–557 (2007)
[Crossref]

G. FitzHarris, P. Marangos, and J. Carroll, “Changes in endoplasmic reticulum structure during mouse oocyte maturation are controlled by the cytoskeleton and cytoplasmic dynein,” Dev. Biol 305, 133–144 (2007).
[Crossref] [PubMed]

C.-H. Yu, S.-P. Tai, C.-T. Kung, I.-J. Wang, H.-C. Yu, H.-J. Huang, W.-J. Lee, Y.-F. Chan, and C.-K. Sun, “In vivo and ex vivo imaging of intra-tissue elastic fibers using third-harmonic-generation microscopy,” Opt. Express 15, 11167–11177 (2007).
[Crossref] [PubMed]

2006 (2)

D. Debarre, W. Supatto, A. M. Pena, A. Fabre, T. Tordjmann, L. Combettes, M. C. Schanne-Klein, and E. Beaurepaire, “Imaging lipid bodies in cells and tissues using third-harmonic generation microscopy,” Nat. Methods 3, 47–53 (2006).
[Crossref]

S.-Y. Chen, C.-S. Hsieh, S.-W. Chu, C.-Y. Ko, Y.-C. Chen, H.-J. Tsai, C.-H. Hu, and C.-K. Sun, “Noninvasive harmonics optical microscopy for long-term observation of embryonic nervous system development in vivo.“J. Biom. Opt 11, 054022 1–8 (2006).

2005 (7)

S.-U. Chen, T.-H. Lee, Y.-R. Lien, Y.-Y. Tsai, L.-J. Chang, and Y.-S. Yang, “Microsuction of blastocoelic fluid before vitrification increased survival and pregnancy of mouse expanded blastocysts, but pretreatment with the cytoskeletal stabilizer did not increase blastocyst survival,” Fertil. Steril 84, 1156–1162 (2005).
[Crossref] [PubMed]

P. Saldeen and P. Sundström “Nuclear status of four-cell preembryos predicts implantation potential in in vitro fertilization treatment cycles,” Fertil. Steril 84, 584–589 (2005).
[Crossref] [PubMed]

Y. Shen, T. Stalf, C. Mehnert, U. Eichenlaub-Ritter, and H.-R. Tinneberg, “High magnitude of light retardation by the zona pellucida is associated with conception cycles,” Hum. Reprod 20, 1596–1606 (2005).
[Crossref] [PubMed]

V. Barzda, C. Greenhalgh, J. A. D. Au, S. Elmore, J. H. van Beek, and J. Squier, “Visualization of mitochondria in cardiomyocytes by simultaneous harmonic generation and fluorescence microscopy,” Opt. Express 13, 8263–8276 (2005).
[Crossref] [PubMed]

V. Barzda, “Visualization of mitochondria in cardiomyocytes by simultaneous harmonic generation and fluorescence microscopy,” Opt. Express 13, 8263–8276 (2005).
[Crossref] [PubMed]

S.-W. Chu, S.-P. Tai, C.-L. Ho, C.-H. Lin, and C.-K Sun, “High-resolution simultaneous three-photon fluorescence and third-harmonic-generation microscopy,” Microsc. Res. Tech 66, 193–197 (2005).
[Crossref] [PubMed]

G. A. Thouas, A. O. Trounson, and G. M. Jones, “Effect of Female Age on Mouse Oocyte Developmental Competence Following Mitochondrial Injury,” Biol. Reprod 73, 366–373 (2005).
[Crossref] [PubMed]

2004 (5)

J. P. de Bruin, M. Dorland, E. R. Spek, G. Posthuma, M. van Haaften, C. W. Looman, and E. R. te Velde, “Agerelated changes in the ultrastructure of the resting follicle pool in human ovaries,” Biol. Reprod 70, 419–424 (2004).
[Crossref]

J. Otsuki, A. Okada, K. Morimoto, Y. Nagai, and H. Kubo “The relationship between pregnancy outcome and smooth endoplasmic reticulum clusters in MII human oocytes,” Hum. Reprod 19, 1591–1597 (2004).
[Crossref] [PubMed]

S.-W. Chu, S.-Y. Chen, G.-W. Chern, T.-H. Tsai, Y.-C. Chen, B.-L. Lin, and C.-K. Sun, “Studies of χ(2)/χ(3) tensors in submicron-scaled bio-tissues by polarization harmonics optical microscopy,” Biophys. J 86, 3914–3922 (2004).
[Crossref] [PubMed]

C. Pelletier, D. L. Keefe, and J. R. Trimarchi, “Noninvasive polarized light microscopy quantitatively distinguishes the multilaminar structure of the zona pellucida of living human eggs and embryos,” Fertil. Steril 81, 850–856 (2004).
[Crossref] [PubMed]

C.-K. Sun, S.-W. Chu, S.-Y. Chen, T.-H. Tsai, T.-M. Liu, C.-Y. Lin, and H.-J. Tsai, “Higher harmonic generation microscopy for developmental biology,” J. Struct. Bio 147, 19–30 (2004).
[Crossref]

2003 (4)

D. F. Albertini and S. L. Barrett, “Oocyte-somatic cell communication,” Reproduction 61 (Suppl), 49–54 (2003).
[PubMed]

G. Fitzharris, P. Marangos, and J. Carroll, “Cell cycle-dependent regulation of structure of endoplasmic reticulum and inositol 1, 4, 5-trisphosphate-induced Ca2+ release in mouse oocytes and embryos,” Mol. Biol. Cell 14, 288–301 (2003).
[Crossref] [PubMed]

S. Cooke, J. P. P. Tyler, and G. L. Driscoll “Meiotic spindle location and identification and its effect on embryonic cleavage plane and early development,” Hum. Reprod 18, 2397–2405 (2003)
[Crossref] [PubMed]

S.-W. Chu, S.-Y. Chen, T.-H. Tsai, T.-M. Liu, C.-Y. Lin, H.-J. Tsai, and C.-K. Sun, “In vivo developmental biology study using noninvasive multi-harmonic generation microscopy,” Opt. Express 11, 3093–3099 (2003).
[Crossref] [PubMed]

2002 (6)

P. Stoller, K. M. Reiser, P. M. Celliers, and A. M. Rubenchik, “Polarization-modulated second harmonic generation in collagen,” Biophys. J 82, 3330–3342 (2002).
[Crossref] [PubMed]

L. Liu and D. L. Keefe, “Ageing-associated aberration in meiosis of oocytes from senescence-accelerated mice,” Hum. Reprod 17, 2678–2685 (2002).
[Crossref] [PubMed]

J. V. Blerkom, P. Davis, V. Mathwig, and S. Alexander, “Domains of high-polarized and low-polarized mitochondria may occur in mouse and human oocytes and early embryos” Hum. Reprod 17, 393–406 (2002).
[Crossref] [PubMed]

R. D. Moreno, G. Schatten, and J. Ramalho-Santos, “Golgi apparatus dynamics during mouse oocyte in vitro maturation: effect of the membrane trafficking inhibitor brefeldin A,” Biol. Reprod 66, 1259–1266 (2002)
[Crossref] [PubMed]

S.-W. Chu, I.-H. Chen, T.-M. Liu, C.-K. Sun, S.-P. Lee, B.-L. Lin, P.-C. Cheng, M.-X. Kuo, D.-J. Lin, and H.- L. Liu, “Nonlinear bio-photonic crystal effects revealed with multimodal nonlinear microscopy,” J. Microsc.-Oxford 208, 190–200 (2002).
[Crossref]

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, 493–508 (2002).
[Crossref]

2001 (2)

M. Terasaki, L. L. Runft, and A. R. Hand, “Changes in organization of the endoplasmic reticulum during Xenopus oocyte maturation and activation,” Mol. Biol. Cell 12, 1103–1116 (2001)
[PubMed]

S.-U. Chen, Y.-R. Lien, Y.-Y. Cheng, H.-F. Chen, H.-N. Ho, and Y.-S. Yang, “Vitrification of mouse oocytes using closed pulled straws (CPS) achieves a high survival and preserves good patterns of meiotic spindles, compared with conventional straws, open pulled straws (OPS) and grids,” Hum. Reprod 16, 2350–2356 (2001).
[PubMed]

2000 (4)

A. C. Millard, D. N. Fittinghoff, P. W. Wiseman, M. Muller, G. J. Brakenhoff, J. A. Squier, and K. R. Wilson, “Three dimensional, third harmonic microscopy of living systems,” Biophys. J 78, 800Plat Part 2 (2000).

S. D. Spandorfer, P. H. Chung, I. Kligman, H. C. Liu, O. K. Davis, and Z. Rosenwal, “An analysis of the effect of age on implantation rates,” J. Assist. Reprod. Genet 17, 303–306 (2000).
[Crossref] [PubMed]

A. Gabrielsen, P.R. Bhatnager, K. Petersen, and S. Lindenberg, “Influence of zona pellucida thickness of human embryos on clinical pregnancy outcome following in vitro fertilization treatment,” J. Assist. Reprod. Genet 17, 323–328 (2000).
[Crossref] [PubMed]

S.-U. Chen, Y.-L. Lien, and H.-F. Chen “Open pulled straws for vitrification of mature mouse oocytes preserve patterns of meiotic spindles and chromosomes better than conventional straws,” Hum. Reprod 15, 2598–2603 (2000).
[Crossref] [PubMed]

1999 (1)

J. M. Squirell, D. L. Wokosin, J. G. White, and B. D. Bavister, “Long-term two-photon fluorescence imaging of mammalian embryos without compromising viability,” Nat. Biotechnol 17, 763–767 (1999).
[Crossref]

1998 (3)

S. Inouè and Oldenbourg R. “Microtubule dynamics in mitotic spindle displayed by polarized light microscopy,” Mol. Biol. Cell 9, 1603–1607 (1998).
[PubMed]

M. Muller, J. Squier, K. R. Wilson, and G. J. Brakenhoff, “3D microscopy of transparent objects using thirdharmonic generation,” J. Microsc.-Oxford 191, 266–274 (1998).
[Crossref]

J. A. Squier, M. Muller, G. J. Brakenhoff, and K. R. Wilson, “Third harmonic generation microscopy,” Opt. Express 3, 315–324 (1998).
[Crossref] [PubMed]

1997 (4)

Y. Barad, H. Eisenberg, M. Horowitz, and Y. Silberberg, “Nonlinear scanning laser microscopy by third harmonic generation,” App. Phy. Lett 70, 922–924 (1997).
[Crossref]

K. Konig, P. T. C. So, W. W. Mantulin, and E. Gratton, “Cellular response to near-infrared femtosecond laser pulses in two-photon microscopes,” Opt. Lett 22, 135–136 (1997).
[Crossref] [PubMed]

D. Keefe, P. Tran, C. Pellegrini, and R. Oldenbourg “Polarized light microscopy and digital image processing identify a multilaminar structure of the hamster zona pellucida,” Hum. Reprod 12, 1250–1252 (1997).
[Crossref] [PubMed]

W. T. Garside, J. R. L. D. Mola, J. A. Bucci, R. W. Tureck, and S. Heyner, “Sequential analysis of zona thickness during in vitro culture of human zygotes: Correlation with embryo quality, age, and implantation,“ Mol. Reprod. Dev 47, 99–104 (1997).
[Crossref] [PubMed]

1996 (1)

Y. Fujino, K. Ozaki, S. Yamamasu, F. Ito, I. Matsuoka, E. Hayashi, H. Nakamura, S. Ogita, E. Sato, and M. Inoue, “DNA fragmentation of oocytes in aged mice,” Hum. Reprod 11, 1480–1483 (1996).
[PubMed]

1995 (2)

L. M. Mehlmann, M. Terasaki, L. A. Jaffe, and D. Kline, “Reorganization of the endoplasmic reticulum during meiotic maturation of the mouse oocyte,” Dev. Biol 170, 607–615 (1995).
[Crossref] [PubMed]

T. Y. F. Tsang, “Optical 3rd-harmonic generation at interfaces,” Phys. Rev A  52, 4116–4125 (1995).
[Crossref]

1994 (2)

D. F. Albertini and V. Rider, “Patterns of intercellular connectivity in the mammalian cumulus-oocyte complex,” Microsc. Res. Tech 27, 125–133 (1994).
[Crossref] [PubMed]

P. M. Motta, S. Makabe, T. Naguro, and S. Correr, “Oocyte follicle cells association during development of human ovarian follicle. A study by high resolution scanning and transmission electron microscopy,” Arch. Histol. Cytol 57, 369–394 (1994).
[Crossref] [PubMed]

1993 (1)

T. Tokura, Y. Noda, Y. Goto, and T. Mori, “Sequential observation of mitochondrial distribution in mouse oocytes and embryos,” J. Assist. Reprod. Genet 10, 417–426 (1993).
[Crossref] [PubMed]

1992 (1)

J. V. Blerkom and G. Henry, “Oocyte dysmorphism and aneuploidy in meiotically mature human oocytes after ovarian stimulation,” Hum. Reprod 7, 379–390 (1992).
[PubMed]

1984 (1)

J. V. Blerkom and M. N. Runner, “Mitochondrial reorganization during resumption of arrested meiosis in the mouse oocyte,” Am. J. Anat 171, 335–355 (1984).
[Crossref] [PubMed]

1981 (1)

B.S. Weakley, P. Webb, and J. L. James, “Cytochemistry of the Golgi apparatus in developing ovarian germ cells of the Syrian hamster,” Cell Tissue Res 220, 349–372 (1981).
[Crossref] [PubMed]

1980 (2)

D. M. Phillips and R. M. Shalgi, “Surface properties of the zona pellucida,” J. Exp. Zool 213, 1–8 (1980).
[Crossref] [PubMed]

J. C. Bleil and P. M. Wassarman, “Structure and function for the zona pellucida: identification and characterization of the proteins of the mouse oocyte’s zona pellucida,” Dev. Biol 76, 185–202 (1980).
[Crossref] [PubMed]

Albertini, D. F.

D. F. Albertini and S. L. Barrett, “Oocyte-somatic cell communication,” Reproduction 61 (Suppl), 49–54 (2003).
[PubMed]

D. F. Albertini and V. Rider, “Patterns of intercellular connectivity in the mammalian cumulus-oocyte complex,” Microsc. Res. Tech 27, 125–133 (1994).
[Crossref] [PubMed]

Alexander, S.

J. V. Blerkom, P. Davis, V. Mathwig, and S. Alexander, “Domains of high-polarized and low-polarized mitochondria may occur in mouse and human oocytes and early embryos” Hum. Reprod 17, 393–406 (2002).
[Crossref] [PubMed]

Au, J. A. D.

Barad, Y.

Y. Barad, H. Eisenberg, M. Horowitz, and Y. Silberberg, “Nonlinear scanning laser microscopy by third harmonic generation,” App. Phy. Lett 70, 922–924 (1997).
[Crossref]

Barrett, S. L.

D. F. Albertini and S. L. Barrett, “Oocyte-somatic cell communication,” Reproduction 61 (Suppl), 49–54 (2003).
[PubMed]

Barzda, V.

Bavister, B. D.

J. M. Squirell, D. L. Wokosin, J. G. White, and B. D. Bavister, “Long-term two-photon fluorescence imaging of mammalian embryos without compromising viability,” Nat. Biotechnol 17, 763–767 (1999).
[Crossref]

Beaurepaire, E.

D. Debarre, W. Supatto, A. M. Pena, A. Fabre, T. Tordjmann, L. Combettes, M. C. Schanne-Klein, and E. Beaurepaire, “Imaging lipid bodies in cells and tissues using third-harmonic generation microscopy,” Nat. Methods 3, 47–53 (2006).
[Crossref]

Bergh, T.

J. Holte, L. Berglund, K. Milton, C. Garello, G. Gennarelli, A. Revelli, and T. Bergh “Construction of an evidence-based integrated morphology cleavage embryo score for implantation potential of embryos scored and transferred on day 2 after oocyte retrieval,” Hum. Reprod 22, 548–557 (2007)
[Crossref]

Berglund, L.

J. Holte, L. Berglund, K. Milton, C. Garello, G. Gennarelli, A. Revelli, and T. Bergh “Construction of an evidence-based integrated morphology cleavage embryo score for implantation potential of embryos scored and transferred on day 2 after oocyte retrieval,” Hum. Reprod 22, 548–557 (2007)
[Crossref]

Bhatnager, P.R.

A. Gabrielsen, P.R. Bhatnager, K. Petersen, and S. Lindenberg, “Influence of zona pellucida thickness of human embryos on clinical pregnancy outcome following in vitro fertilization treatment,” J. Assist. Reprod. Genet 17, 323–328 (2000).
[Crossref] [PubMed]

Biggs, D.

M. Shribak, J. LaFountain, D. Biggs, and S. Inouè, “Quantitative orientation-independent differential interference contrast (DIC) microscopy coupled with orientation-independent polarization microscopy,” Microsc. Microanal 13, 10–11 (2007).
[PubMed]

Bleil, J. C.

J. C. Bleil and P. M. Wassarman, “Structure and function for the zona pellucida: identification and characterization of the proteins of the mouse oocyte’s zona pellucida,” Dev. Biol 76, 185–202 (1980).
[Crossref] [PubMed]

Blerkom, J. V.

J. V. Blerkom, P. Davis, V. Mathwig, and S. Alexander, “Domains of high-polarized and low-polarized mitochondria may occur in mouse and human oocytes and early embryos” Hum. Reprod 17, 393–406 (2002).
[Crossref] [PubMed]

J. V. Blerkom and G. Henry, “Oocyte dysmorphism and aneuploidy in meiotically mature human oocytes after ovarian stimulation,” Hum. Reprod 7, 379–390 (1992).
[PubMed]

J. V. Blerkom and M. N. Runner, “Mitochondrial reorganization during resumption of arrested meiosis in the mouse oocyte,” Am. J. Anat 171, 335–355 (1984).
[Crossref] [PubMed]

Brakenhoff, G. J.

A. C. Millard, D. N. Fittinghoff, P. W. Wiseman, M. Muller, G. J. Brakenhoff, J. A. Squier, and K. R. Wilson, “Three dimensional, third harmonic microscopy of living systems,” Biophys. J 78, 800Plat Part 2 (2000).

J. A. Squier, M. Muller, G. J. Brakenhoff, and K. R. Wilson, “Third harmonic generation microscopy,” Opt. Express 3, 315–324 (1998).
[Crossref] [PubMed]

M. Muller, J. Squier, K. R. Wilson, and G. J. Brakenhoff, “3D microscopy of transparent objects using thirdharmonic generation,” J. Microsc.-Oxford 191, 266–274 (1998).
[Crossref]

Bucci, J. A.

W. T. Garside, J. R. L. D. Mola, J. A. Bucci, R. W. Tureck, and S. Heyner, “Sequential analysis of zona thickness during in vitro culture of human zygotes: Correlation with embryo quality, age, and implantation,“ Mol. Reprod. Dev 47, 99–104 (1997).
[Crossref] [PubMed]

Campagnola, P. J.

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, 493–508 (2002).
[Crossref]

Carroll, J.

G. FitzHarris, P. Marangos, and J. Carroll, “Changes in endoplasmic reticulum structure during mouse oocyte maturation are controlled by the cytoskeleton and cytoplasmic dynein,” Dev. Biol 305, 133–144 (2007).
[Crossref] [PubMed]

G. Fitzharris, P. Marangos, and J. Carroll, “Cell cycle-dependent regulation of structure of endoplasmic reticulum and inositol 1, 4, 5-trisphosphate-induced Ca2+ release in mouse oocytes and embryos,” Mol. Biol. Cell 14, 288–301 (2003).
[Crossref] [PubMed]

Celliers, P. M.

P. Stoller, K. M. Reiser, P. M. Celliers, and A. M. Rubenchik, “Polarization-modulated second harmonic generation in collagen,” Biophys. J 82, 3330–3342 (2002).
[Crossref] [PubMed]

Chan, Y.-F.

C.-H. Yu, S.-P. Tai, C.-T. Kung, W.-J. Lee, Y.-F. Chan, H.-L. Liu, J.-Y. Lyu, and C.-K. Sun, “Molecular thirdharmonic- generation microscopy through resonance enhancement with absorbing dye,” Opt. Lett 33, 387–389 (2008).
[Crossref] [PubMed]

C.-H. Yu, S.-P. Tai, C.-T. Kung, I.-J. Wang, H.-C. Yu, H.-J. Huang, W.-J. Lee, Y.-F. Chan, and C.-K. Sun, “In vivo and ex vivo imaging of intra-tissue elastic fibers using third-harmonic-generation microscopy,” Opt. Express 15, 11167–11177 (2007).
[Crossref] [PubMed]

Chang, L.-J.

S.-U. Chen, T.-H. Lee, Y.-R. Lien, Y.-Y. Tsai, L.-J. Chang, and Y.-S. Yang, “Microsuction of blastocoelic fluid before vitrification increased survival and pregnancy of mouse expanded blastocysts, but pretreatment with the cytoskeletal stabilizer did not increase blastocyst survival,” Fertil. Steril 84, 1156–1162 (2005).
[Crossref] [PubMed]

Chen, H.-F.

S.-U. Chen, Y.-R. Lien, Y.-Y. Cheng, H.-F. Chen, H.-N. Ho, and Y.-S. Yang, “Vitrification of mouse oocytes using closed pulled straws (CPS) achieves a high survival and preserves good patterns of meiotic spindles, compared with conventional straws, open pulled straws (OPS) and grids,” Hum. Reprod 16, 2350–2356 (2001).
[PubMed]

S.-U. Chen, Y.-L. Lien, and H.-F. Chen “Open pulled straws for vitrification of mature mouse oocytes preserve patterns of meiotic spindles and chromosomes better than conventional straws,” Hum. Reprod 15, 2598–2603 (2000).
[Crossref] [PubMed]

Chen, I.-H.

S.-W. Chu, I.-H. Chen, T.-M. Liu, C.-K. Sun, S.-P. Lee, B.-L. Lin, P.-C. Cheng, M.-X. Kuo, D.-J. Lin, and H.- L. Liu, “Nonlinear bio-photonic crystal effects revealed with multimodal nonlinear microscopy,” J. Microsc.-Oxford 208, 190–200 (2002).
[Crossref]

Chen, S.-U.

S.-U. Chen, T.-H. Lee, Y.-R. Lien, Y.-Y. Tsai, L.-J. Chang, and Y.-S. Yang, “Microsuction of blastocoelic fluid before vitrification increased survival and pregnancy of mouse expanded blastocysts, but pretreatment with the cytoskeletal stabilizer did not increase blastocyst survival,” Fertil. Steril 84, 1156–1162 (2005).
[Crossref] [PubMed]

S.-U. Chen, Y.-R. Lien, Y.-Y. Cheng, H.-F. Chen, H.-N. Ho, and Y.-S. Yang, “Vitrification of mouse oocytes using closed pulled straws (CPS) achieves a high survival and preserves good patterns of meiotic spindles, compared with conventional straws, open pulled straws (OPS) and grids,” Hum. Reprod 16, 2350–2356 (2001).
[PubMed]

S.-U. Chen, Y.-L. Lien, and H.-F. Chen “Open pulled straws for vitrification of mature mouse oocytes preserve patterns of meiotic spindles and chromosomes better than conventional straws,” Hum. Reprod 15, 2598–2603 (2000).
[Crossref] [PubMed]

Chen, S.-Y.

S.-Y. Chen, C.-S. Hsieh, S.-W. Chu, C.-Y. Ko, Y.-C. Chen, H.-J. Tsai, C.-H. Hu, and C.-K. Sun, “Noninvasive harmonics optical microscopy for long-term observation of embryonic nervous system development in vivo.“J. Biom. Opt 11, 054022 1–8 (2006).

C.-K. Sun, S.-W. Chu, S.-Y. Chen, T.-H. Tsai, T.-M. Liu, C.-Y. Lin, and H.-J. Tsai, “Higher harmonic generation microscopy for developmental biology,” J. Struct. Bio 147, 19–30 (2004).
[Crossref]

S.-W. Chu, S.-Y. Chen, G.-W. Chern, T.-H. Tsai, Y.-C. Chen, B.-L. Lin, and C.-K. Sun, “Studies of χ(2)/χ(3) tensors in submicron-scaled bio-tissues by polarization harmonics optical microscopy,” Biophys. J 86, 3914–3922 (2004).
[Crossref] [PubMed]

S.-W. Chu, S.-Y. Chen, T.-H. Tsai, T.-M. Liu, C.-Y. Lin, H.-J. Tsai, and C.-K. Sun, “In vivo developmental biology study using noninvasive multi-harmonic generation microscopy,” Opt. Express 11, 3093–3099 (2003).
[Crossref] [PubMed]

Chen, Y.-C.

S.-Y. Chen, C.-S. Hsieh, S.-W. Chu, C.-Y. Ko, Y.-C. Chen, H.-J. Tsai, C.-H. Hu, and C.-K. Sun, “Noninvasive harmonics optical microscopy for long-term observation of embryonic nervous system development in vivo.“J. Biom. Opt 11, 054022 1–8 (2006).

S.-W. Chu, S.-Y. Chen, G.-W. Chern, T.-H. Tsai, Y.-C. Chen, B.-L. Lin, and C.-K. Sun, “Studies of χ(2)/χ(3) tensors in submicron-scaled bio-tissues by polarization harmonics optical microscopy,” Biophys. J 86, 3914–3922 (2004).
[Crossref] [PubMed]

Cheng, P.-C.

S.-W. Chu, I.-H. Chen, T.-M. Liu, C.-K. Sun, S.-P. Lee, B.-L. Lin, P.-C. Cheng, M.-X. Kuo, D.-J. Lin, and H.- L. Liu, “Nonlinear bio-photonic crystal effects revealed with multimodal nonlinear microscopy,” J. Microsc.-Oxford 208, 190–200 (2002).
[Crossref]

Cheng, Y.-Y.

S.-U. Chen, Y.-R. Lien, Y.-Y. Cheng, H.-F. Chen, H.-N. Ho, and Y.-S. Yang, “Vitrification of mouse oocytes using closed pulled straws (CPS) achieves a high survival and preserves good patterns of meiotic spindles, compared with conventional straws, open pulled straws (OPS) and grids,” Hum. Reprod 16, 2350–2356 (2001).
[PubMed]

Chern, G.-W.

S.-W. Chu, S.-Y. Chen, G.-W. Chern, T.-H. Tsai, Y.-C. Chen, B.-L. Lin, and C.-K. Sun, “Studies of χ(2)/χ(3) tensors in submicron-scaled bio-tissues by polarization harmonics optical microscopy,” Biophys. J 86, 3914–3922 (2004).
[Crossref] [PubMed]

Chu, S.-W.

S.-Y. Chen, C.-S. Hsieh, S.-W. Chu, C.-Y. Ko, Y.-C. Chen, H.-J. Tsai, C.-H. Hu, and C.-K. Sun, “Noninvasive harmonics optical microscopy for long-term observation of embryonic nervous system development in vivo.“J. Biom. Opt 11, 054022 1–8 (2006).

S.-W. Chu, S.-P. Tai, C.-L. Ho, C.-H. Lin, and C.-K Sun, “High-resolution simultaneous three-photon fluorescence and third-harmonic-generation microscopy,” Microsc. Res. Tech 66, 193–197 (2005).
[Crossref] [PubMed]

S.-W. Chu, S.-Y. Chen, G.-W. Chern, T.-H. Tsai, Y.-C. Chen, B.-L. Lin, and C.-K. Sun, “Studies of χ(2)/χ(3) tensors in submicron-scaled bio-tissues by polarization harmonics optical microscopy,” Biophys. J 86, 3914–3922 (2004).
[Crossref] [PubMed]

C.-K. Sun, S.-W. Chu, S.-Y. Chen, T.-H. Tsai, T.-M. Liu, C.-Y. Lin, and H.-J. Tsai, “Higher harmonic generation microscopy for developmental biology,” J. Struct. Bio 147, 19–30 (2004).
[Crossref]

S.-W. Chu, S.-Y. Chen, T.-H. Tsai, T.-M. Liu, C.-Y. Lin, H.-J. Tsai, and C.-K. Sun, “In vivo developmental biology study using noninvasive multi-harmonic generation microscopy,” Opt. Express 11, 3093–3099 (2003).
[Crossref] [PubMed]

S.-W. Chu, I.-H. Chen, T.-M. Liu, C.-K. Sun, S.-P. Lee, B.-L. Lin, P.-C. Cheng, M.-X. Kuo, D.-J. Lin, and H.- L. Liu, “Nonlinear bio-photonic crystal effects revealed with multimodal nonlinear microscopy,” J. Microsc.-Oxford 208, 190–200 (2002).
[Crossref]

Chung, P. H.

S. D. Spandorfer, P. H. Chung, I. Kligman, H. C. Liu, O. K. Davis, and Z. Rosenwal, “An analysis of the effect of age on implantation rates,” J. Assist. Reprod. Genet 17, 303–306 (2000).
[Crossref] [PubMed]

Combettes, L.

D. Debarre, W. Supatto, A. M. Pena, A. Fabre, T. Tordjmann, L. Combettes, M. C. Schanne-Klein, and E. Beaurepaire, “Imaging lipid bodies in cells and tissues using third-harmonic generation microscopy,” Nat. Methods 3, 47–53 (2006).
[Crossref]

Cooke, S.

S. Cooke, J. P. P. Tyler, and G. L. Driscoll “Meiotic spindle location and identification and its effect on embryonic cleavage plane and early development,” Hum. Reprod 18, 2397–2405 (2003)
[Crossref] [PubMed]

Correr, S.

P. M. Motta, S. Makabe, T. Naguro, and S. Correr, “Oocyte follicle cells association during development of human ovarian follicle. A study by high resolution scanning and transmission electron microscopy,” Arch. Histol. Cytol 57, 369–394 (1994).
[Crossref] [PubMed]

Davis, O. K.

S. D. Spandorfer, P. H. Chung, I. Kligman, H. C. Liu, O. K. Davis, and Z. Rosenwal, “An analysis of the effect of age on implantation rates,” J. Assist. Reprod. Genet 17, 303–306 (2000).
[Crossref] [PubMed]

Davis, P.

J. V. Blerkom, P. Davis, V. Mathwig, and S. Alexander, “Domains of high-polarized and low-polarized mitochondria may occur in mouse and human oocytes and early embryos” Hum. Reprod 17, 393–406 (2002).
[Crossref] [PubMed]

de Bruin, J. P.

J. P. de Bruin, M. Dorland, E. R. Spek, G. Posthuma, M. van Haaften, C. W. Looman, and E. R. te Velde, “Agerelated changes in the ultrastructure of the resting follicle pool in human ovaries,” Biol. Reprod 70, 419–424 (2004).
[Crossref]

Debarre, D.

D. Debarre, W. Supatto, A. M. Pena, A. Fabre, T. Tordjmann, L. Combettes, M. C. Schanne-Klein, and E. Beaurepaire, “Imaging lipid bodies in cells and tissues using third-harmonic generation microscopy,” Nat. Methods 3, 47–53 (2006).
[Crossref]

Dorland, M.

J. P. de Bruin, M. Dorland, E. R. Spek, G. Posthuma, M. van Haaften, C. W. Looman, and E. R. te Velde, “Agerelated changes in the ultrastructure of the resting follicle pool in human ovaries,” Biol. Reprod 70, 419–424 (2004).
[Crossref]

Driscoll, G. L.

S. Cooke, J. P. P. Tyler, and G. L. Driscoll “Meiotic spindle location and identification and its effect on embryonic cleavage plane and early development,” Hum. Reprod 18, 2397–2405 (2003)
[Crossref] [PubMed]

Eichenlaub-Ritter, U.

Y. Shen, T. Stalf, C. Mehnert, U. Eichenlaub-Ritter, and H.-R. Tinneberg, “High magnitude of light retardation by the zona pellucida is associated with conception cycles,” Hum. Reprod 20, 1596–1606 (2005).
[Crossref] [PubMed]

Eisenberg, H.

Y. Barad, H. Eisenberg, M. Horowitz, and Y. Silberberg, “Nonlinear scanning laser microscopy by third harmonic generation,” App. Phy. Lett 70, 922–924 (1997).
[Crossref]

Elmore, S.

Fabre, A.

D. Debarre, W. Supatto, A. M. Pena, A. Fabre, T. Tordjmann, L. Combettes, M. C. Schanne-Klein, and E. Beaurepaire, “Imaging lipid bodies in cells and tissues using third-harmonic generation microscopy,” Nat. Methods 3, 47–53 (2006).
[Crossref]

Fittinghoff, D. N.

A. C. Millard, D. N. Fittinghoff, P. W. Wiseman, M. Muller, G. J. Brakenhoff, J. A. Squier, and K. R. Wilson, “Three dimensional, third harmonic microscopy of living systems,” Biophys. J 78, 800Plat Part 2 (2000).

FitzHarris, G.

G. FitzHarris, P. Marangos, and J. Carroll, “Changes in endoplasmic reticulum structure during mouse oocyte maturation are controlled by the cytoskeleton and cytoplasmic dynein,” Dev. Biol 305, 133–144 (2007).
[Crossref] [PubMed]

G. Fitzharris, P. Marangos, and J. Carroll, “Cell cycle-dependent regulation of structure of endoplasmic reticulum and inositol 1, 4, 5-trisphosphate-induced Ca2+ release in mouse oocytes and embryos,” Mol. Biol. Cell 14, 288–301 (2003).
[Crossref] [PubMed]

Fujino, Y.

Y. Fujino, K. Ozaki, S. Yamamasu, F. Ito, I. Matsuoka, E. Hayashi, H. Nakamura, S. Ogita, E. Sato, and M. Inoue, “DNA fragmentation of oocytes in aged mice,” Hum. Reprod 11, 1480–1483 (1996).
[PubMed]

Gabrielsen, A.

A. Gabrielsen, P.R. Bhatnager, K. Petersen, and S. Lindenberg, “Influence of zona pellucida thickness of human embryos on clinical pregnancy outcome following in vitro fertilization treatment,” J. Assist. Reprod. Genet 17, 323–328 (2000).
[Crossref] [PubMed]

Garello, C.

J. Holte, L. Berglund, K. Milton, C. Garello, G. Gennarelli, A. Revelli, and T. Bergh “Construction of an evidence-based integrated morphology cleavage embryo score for implantation potential of embryos scored and transferred on day 2 after oocyte retrieval,” Hum. Reprod 22, 548–557 (2007)
[Crossref]

Garside, W. T.

W. T. Garside, J. R. L. D. Mola, J. A. Bucci, R. W. Tureck, and S. Heyner, “Sequential analysis of zona thickness during in vitro culture of human zygotes: Correlation with embryo quality, age, and implantation,“ Mol. Reprod. Dev 47, 99–104 (1997).
[Crossref] [PubMed]

Gennarelli, G.

J. Holte, L. Berglund, K. Milton, C. Garello, G. Gennarelli, A. Revelli, and T. Bergh “Construction of an evidence-based integrated morphology cleavage embryo score for implantation potential of embryos scored and transferred on day 2 after oocyte retrieval,” Hum. Reprod 22, 548–557 (2007)
[Crossref]

Goto, Y.

T. Tokura, Y. Noda, Y. Goto, and T. Mori, “Sequential observation of mitochondrial distribution in mouse oocytes and embryos,” J. Assist. Reprod. Genet 10, 417–426 (1993).
[Crossref] [PubMed]

Gratton, E.

K. Konig, P. T. C. So, W. W. Mantulin, and E. Gratton, “Cellular response to near-infrared femtosecond laser pulses in two-photon microscopes,” Opt. Lett 22, 135–136 (1997).
[Crossref] [PubMed]

Greenhalgh, C.

Hand, A. R.

M. Terasaki, L. L. Runft, and A. R. Hand, “Changes in organization of the endoplasmic reticulum during Xenopus oocyte maturation and activation,” Mol. Biol. Cell 12, 1103–1116 (2001)
[PubMed]

Hayashi, E.

Y. Fujino, K. Ozaki, S. Yamamasu, F. Ito, I. Matsuoka, E. Hayashi, H. Nakamura, S. Ogita, E. Sato, and M. Inoue, “DNA fragmentation of oocytes in aged mice,” Hum. Reprod 11, 1480–1483 (1996).
[PubMed]

Henry, G.

J. V. Blerkom and G. Henry, “Oocyte dysmorphism and aneuploidy in meiotically mature human oocytes after ovarian stimulation,” Hum. Reprod 7, 379–390 (1992).
[PubMed]

Heyner, S.

W. T. Garside, J. R. L. D. Mola, J. A. Bucci, R. W. Tureck, and S. Heyner, “Sequential analysis of zona thickness during in vitro culture of human zygotes: Correlation with embryo quality, age, and implantation,“ Mol. Reprod. Dev 47, 99–104 (1997).
[Crossref] [PubMed]

Hinkle, D. E.

D. E. Hinkle, W. Wiersma, and S. G. JursApplied Statistics for the Behavioral Sciences, 2nd ed., (Houghton Mifflin Co.,1988).

Ho, C.-L.

S.-W. Chu, S.-P. Tai, C.-L. Ho, C.-H. Lin, and C.-K Sun, “High-resolution simultaneous three-photon fluorescence and third-harmonic-generation microscopy,” Microsc. Res. Tech 66, 193–197 (2005).
[Crossref] [PubMed]

Ho, H.-N.

S.-U. Chen, Y.-R. Lien, Y.-Y. Cheng, H.-F. Chen, H.-N. Ho, and Y.-S. Yang, “Vitrification of mouse oocytes using closed pulled straws (CPS) achieves a high survival and preserves good patterns of meiotic spindles, compared with conventional straws, open pulled straws (OPS) and grids,” Hum. Reprod 16, 2350–2356 (2001).
[PubMed]

Holte, J.

J. Holte, L. Berglund, K. Milton, C. Garello, G. Gennarelli, A. Revelli, and T. Bergh “Construction of an evidence-based integrated morphology cleavage embryo score for implantation potential of embryos scored and transferred on day 2 after oocyte retrieval,” Hum. Reprod 22, 548–557 (2007)
[Crossref]

Hoppe, P. E.

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, 493–508 (2002).
[Crossref]

Horowitz, M.

Y. Barad, H. Eisenberg, M. Horowitz, and Y. Silberberg, “Nonlinear scanning laser microscopy by third harmonic generation,” App. Phy. Lett 70, 922–924 (1997).
[Crossref]

Hsieh, C.-S.

S.-Y. Chen, C.-S. Hsieh, S.-W. Chu, C.-Y. Ko, Y.-C. Chen, H.-J. Tsai, C.-H. Hu, and C.-K. Sun, “Noninvasive harmonics optical microscopy for long-term observation of embryonic nervous system development in vivo.“J. Biom. Opt 11, 054022 1–8 (2006).

Hu, C.-H.

S.-Y. Chen, C.-S. Hsieh, S.-W. Chu, C.-Y. Ko, Y.-C. Chen, H.-J. Tsai, C.-H. Hu, and C.-K. Sun, “Noninvasive harmonics optical microscopy for long-term observation of embryonic nervous system development in vivo.“J. Biom. Opt 11, 054022 1–8 (2006).

Huang, H.-J.

Inoue, M.

Y. Fujino, K. Ozaki, S. Yamamasu, F. Ito, I. Matsuoka, E. Hayashi, H. Nakamura, S. Ogita, E. Sato, and M. Inoue, “DNA fragmentation of oocytes in aged mice,” Hum. Reprod 11, 1480–1483 (1996).
[PubMed]

Inouè, S.

M. Shribak, J. LaFountain, D. Biggs, and S. Inouè, “Quantitative orientation-independent differential interference contrast (DIC) microscopy coupled with orientation-independent polarization microscopy,” Microsc. Microanal 13, 10–11 (2007).
[PubMed]

S. Inouè and Oldenbourg R. “Microtubule dynamics in mitotic spindle displayed by polarized light microscopy,” Mol. Biol. Cell 9, 1603–1607 (1998).
[PubMed]

Ito, F.

Y. Fujino, K. Ozaki, S. Yamamasu, F. Ito, I. Matsuoka, E. Hayashi, H. Nakamura, S. Ogita, E. Sato, and M. Inoue, “DNA fragmentation of oocytes in aged mice,” Hum. Reprod 11, 1480–1483 (1996).
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A. C. Millard, D. N. Fittinghoff, P. W. Wiseman, M. Muller, G. J. Brakenhoff, J. A. Squier, and K. R. Wilson, “Three dimensional, third harmonic microscopy of living systems,” Biophys. J 78, 800Plat Part 2 (2000).

J. A. Squier, M. Muller, G. J. Brakenhoff, and K. R. Wilson, “Third harmonic generation microscopy,” Opt. Express 3, 315–324 (1998).
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J. M. Squirell, D. L. Wokosin, J. G. White, and B. D. Bavister, “Long-term two-photon fluorescence imaging of mammalian embryos without compromising viability,” Nat. Biotechnol 17, 763–767 (1999).
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Y. Shen, T. Stalf, C. Mehnert, U. Eichenlaub-Ritter, and H.-R. Tinneberg, “High magnitude of light retardation by the zona pellucida is associated with conception cycles,” Hum. Reprod 20, 1596–1606 (2005).
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Stoller, P.

P. Stoller, K. M. Reiser, P. M. Celliers, and A. M. Rubenchik, “Polarization-modulated second harmonic generation in collagen,” Biophys. J 82, 3330–3342 (2002).
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Sun, C.-K

S.-W. Chu, S.-P. Tai, C.-L. Ho, C.-H. Lin, and C.-K Sun, “High-resolution simultaneous three-photon fluorescence and third-harmonic-generation microscopy,” Microsc. Res. Tech 66, 193–197 (2005).
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Sun, C.-K.

C.-H. Yu, S.-P. Tai, C.-T. Kung, W.-J. Lee, Y.-F. Chan, H.-L. Liu, J.-Y. Lyu, and C.-K. Sun, “Molecular thirdharmonic- generation microscopy through resonance enhancement with absorbing dye,” Opt. Lett 33, 387–389 (2008).
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C.-H. Yu, S.-P. Tai, C.-T. Kung, I.-J. Wang, H.-C. Yu, H.-J. Huang, W.-J. Lee, Y.-F. Chan, and C.-K. Sun, “In vivo and ex vivo imaging of intra-tissue elastic fibers using third-harmonic-generation microscopy,” Opt. Express 15, 11167–11177 (2007).
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C.-K. Sun, S.-W. Chu, S.-Y. Chen, T.-H. Tsai, T.-M. Liu, C.-Y. Lin, and H.-J. Tsai, “Higher harmonic generation microscopy for developmental biology,” J. Struct. Bio 147, 19–30 (2004).
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S.-W. Chu, S.-Y. Chen, T.-H. Tsai, T.-M. Liu, C.-Y. Lin, H.-J. Tsai, and C.-K. Sun, “In vivo developmental biology study using noninvasive multi-harmonic generation microscopy,” Opt. Express 11, 3093–3099 (2003).
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S.-W. Chu, I.-H. Chen, T.-M. Liu, C.-K. Sun, S.-P. Lee, B.-L. Lin, P.-C. Cheng, M.-X. Kuo, D.-J. Lin, and H.- L. Liu, “Nonlinear bio-photonic crystal effects revealed with multimodal nonlinear microscopy,” J. Microsc.-Oxford 208, 190–200 (2002).
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P. Saldeen and P. Sundström “Nuclear status of four-cell preembryos predicts implantation potential in in vitro fertilization treatment cycles,” Fertil. Steril 84, 584–589 (2005).
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C.-H. Yu, S.-P. Tai, C.-T. Kung, W.-J. Lee, Y.-F. Chan, H.-L. Liu, J.-Y. Lyu, and C.-K. Sun, “Molecular thirdharmonic- generation microscopy through resonance enhancement with absorbing dye,” Opt. Lett 33, 387–389 (2008).
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S.-W. Chu, S.-P. Tai, C.-L. Ho, C.-H. Lin, and C.-K Sun, “High-resolution simultaneous three-photon fluorescence and third-harmonic-generation microscopy,” Microsc. Res. Tech 66, 193–197 (2005).
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J. P. de Bruin, M. Dorland, E. R. Spek, G. Posthuma, M. van Haaften, C. W. Looman, and E. R. te Velde, “Agerelated changes in the ultrastructure of the resting follicle pool in human ovaries,” Biol. Reprod 70, 419–424 (2004).
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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, 493–508 (2002).
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Y. Shen, T. Stalf, C. Mehnert, U. Eichenlaub-Ritter, and H.-R. Tinneberg, “High magnitude of light retardation by the zona pellucida is associated with conception cycles,” Hum. Reprod 20, 1596–1606 (2005).
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C. Pelletier, D. L. Keefe, and J. R. Trimarchi, “Noninvasive polarized light microscopy quantitatively distinguishes the multilaminar structure of the zona pellucida of living human eggs and embryos,” Fertil. Steril 81, 850–856 (2004).
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C.-K. Sun, S.-W. Chu, S.-Y. Chen, T.-H. Tsai, T.-M. Liu, C.-Y. Lin, and H.-J. Tsai, “Higher harmonic generation microscopy for developmental biology,” J. Struct. Bio 147, 19–30 (2004).
[Crossref]

S.-W. Chu, S.-Y. Chen, T.-H. Tsai, T.-M. Liu, C.-Y. Lin, H.-J. Tsai, and C.-K. Sun, “In vivo developmental biology study using noninvasive multi-harmonic generation microscopy,” Opt. Express 11, 3093–3099 (2003).
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C.-K. Sun, S.-W. Chu, S.-Y. Chen, T.-H. Tsai, T.-M. Liu, C.-Y. Lin, and H.-J. Tsai, “Higher harmonic generation microscopy for developmental biology,” J. Struct. Bio 147, 19–30 (2004).
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J. P. de Bruin, M. Dorland, E. R. Spek, G. Posthuma, M. van Haaften, C. W. Looman, and E. R. te Velde, “Agerelated changes in the ultrastructure of the resting follicle pool in human ovaries,” Biol. Reprod 70, 419–424 (2004).
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J. M. Squirell, D. L. Wokosin, J. G. White, and B. D. Bavister, “Long-term two-photon fluorescence imaging of mammalian embryos without compromising viability,” Nat. Biotechnol 17, 763–767 (1999).
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M. Muller, J. Squier, K. R. Wilson, and G. J. Brakenhoff, “3D microscopy of transparent objects using thirdharmonic generation,” J. Microsc.-Oxford 191, 266–274 (1998).
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A. C. Millard, D. N. Fittinghoff, P. W. Wiseman, M. Muller, G. J. Brakenhoff, J. A. Squier, and K. R. Wilson, “Three dimensional, third harmonic microscopy of living systems,” Biophys. J 78, 800Plat Part 2 (2000).

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J. M. Squirell, D. L. Wokosin, J. G. White, and B. D. Bavister, “Long-term two-photon fluorescence imaging of mammalian embryos without compromising viability,” Nat. Biotechnol 17, 763–767 (1999).
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A. C. Millard, D. N. Fittinghoff, P. W. Wiseman, M. Muller, G. J. Brakenhoff, J. A. Squier, and K. R. Wilson, “Three dimensional, third harmonic microscopy of living systems,” Biophys. J 78, 800Plat Part 2 (2000).

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, 493–508 (2002).
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P. Stoller, K. M. Reiser, P. M. Celliers, and A. M. Rubenchik, “Polarization-modulated second harmonic generation in collagen,” Biophys. J 82, 3330–3342 (2002).
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S.-W. Chu, S.-Y. Chen, G.-W. Chern, T.-H. Tsai, Y.-C. Chen, B.-L. Lin, and C.-K. Sun, “Studies of χ(2)/χ(3) tensors in submicron-scaled bio-tissues by polarization harmonics optical microscopy,” Biophys. J 86, 3914–3922 (2004).
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Cell Tissue Res (1)

B.S. Weakley, P. Webb, and J. L. James, “Cytochemistry of the Golgi apparatus in developing ovarian germ cells of the Syrian hamster,” Cell Tissue Res 220, 349–372 (1981).
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L. M. Mehlmann, M. Terasaki, L. A. Jaffe, and D. Kline, “Reorganization of the endoplasmic reticulum during meiotic maturation of the mouse oocyte,” Dev. Biol 170, 607–615 (1995).
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S.-U. Chen, T.-H. Lee, Y.-R. Lien, Y.-Y. Tsai, L.-J. Chang, and Y.-S. Yang, “Microsuction of blastocoelic fluid before vitrification increased survival and pregnancy of mouse expanded blastocysts, but pretreatment with the cytoskeletal stabilizer did not increase blastocyst survival,” Fertil. Steril 84, 1156–1162 (2005).
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C.-K. Sun, S.-W. Chu, S.-Y. Chen, T.-H. Tsai, T.-M. Liu, C.-Y. Lin, and H.-J. Tsai, “Higher harmonic generation microscopy for developmental biology,” J. Struct. Bio 147, 19–30 (2004).
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Figures (9)

Fig. 1.
Fig. 1.

Depth-resolved section series with combined SHG and THG signals inside a live mouse embryo at the 2–cells stage. (A) – (H) were acquired at imaging depths from 0μm to 63μm relative to (A) with a step of 9μm. The SHG and THG signals are denoted by green and blue colors, respectively. Scale bar: 60μm.

Fig. 2.
Fig. 2.

HGM sectioned images of the in vitro cultured mouse (A) oocyte and (B)–(I) embryos. (A) The SHG signals reveal the spindle fibers (indicated by the yellow arrow) and the zona pellucida (indicated by the white arrow) of the oocyte, while the THG signals reveals the cell membrane, the organelles, and the polar body (indicated by the red arrow). (B) and (C) are images of the same mouse embryo at the 2P stage taken at different depths. The white arrows indicate the two pronuclei. (D)–(H) are images of mouse embryos at the 2–cells, 4–cells, 8–cells uncompacted, 8–cells compacted, and morula stages, respectively. (I) After cavitation, the embryo developed the blastocoel (indicated by the yellow arrow), the trophectoderm (indicated by the white arrow), the inner cell mass (indicated by the red arrow), and turned into a blastocyst. The SHG and THG signals are denoted by green and blue colors, respectively. Scale bar: 60μm

Fig. 3.
Fig. 3.

Normalized nonlinear emission spectra from the organelles labeled by 5 different dyes. The black, red, and blue curves are the spectra measured from the BODIPY FL C5–ceramide labeled Golgi apparatus, ER–Tracker Blue-White DPX labeled ER, and MitoTracker Red CMH2XRos labeled mitochondria, respectively. The green and light blue curves are spectra measured from lysosomes labeled by LysoSensor Green DND189 and LysoTracker Red Lysosomal Probe, respectively. The peak at 410nm represents the THG signals.

Fig 4.
Fig 4.

(A) (D), (G), (J), (M) THG (shown in blue) and (B), (E), (H), (K), (N) multiphoton fluorescence (shown in red) images of in vitro stained mouse oocytes. (C), (F), (I), (L), (O) are the combined THG/fluorescence images. (A)–(C) are images of an oocyte stained with BODIPY FL C5–ceramide. (D)–(F) are images of an oocyte stained with ER-Tracker Blue- White DPX. (G)–(I) are images of an oocyte stained with MitoTracker Red CM-H2XRos. (J)–(L) are images of an oocyte stained with LysoSensor Green DND189. (M)–(O) are images of an oocyte stained with LysoTracker Red Lysosomal Probe. Scale bar: 60μm.

Fig. 5.
Fig. 5.

Pearson’s correlation of THG and fluorescence signals revealed from mouse (A) oocytes and (B) embryos stained with BF: BODIPY FL C5–ceramide, EB: ER-Tracker Blue-White DPX, MR: MitoTracker Red CM-H2XRos, LG: LysoSensor Green DND189, and LR: LysoTracker Red Lysosomal Probe, respectively.

Fig. 6.
Fig. 6.

(A) SHG image of a mouse embryo at the morula stage. (B) Enlarged image corresponding to the squared area in (A), which can distinguish the three layers of zona pellucida. (C) The vertical position dependent SHG intensity after integration along the horizontal direction. Scale bar: 60μm.

Fig. 7.
Fig. 7.

(A) In vitro HGM image sectioned through the center of a mouse oocyte. Following (A), (B) and (C) show the SHG intensity of the (B) IL and (C) OL as a function of the angle θ between the laser polarization and the normal vector to the surface of the zona pellucida. Red lines are fitting curves following Eq. (3). Scale bar: 60μm.

Fig 8.
Fig 8.

Born mice of the experiment set. Among the implanted 18 embryos, 12 mice were hatched, with a ratio similar to the control set.

Fig. 9.
Fig. 9.

In vitro HGM images of oocytes obtained from (A) pubertal (4–6 weeks) and (B), (C) aging (> 8 months) mice. Scale bar: 60μm.

Equations (3)

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r = i = 1 n ( X i X - ) ( Y i Y - ) ( n 1 ) S X S Y ,
P ( 2 ) = a ŝ ( ŝ E ) 2 + b ŝ E 2 + c E ( ŝ E )
I SHG E 4 { ( d 31 sin 2 θ + d 33 cos 2 θ ) 2 + d 15 2 sin 2 ( 2 θ ) } ,

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