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Second harmonic properties of tumor collagen: determining the structural relationship between reactive stroma and healthy stroma.

Xiaoxing Han, Ryan M. Burke, Martha L. Zettel, Ping Tang, and Edward B. Brown

Open Access Open Access

Abstract

We utilize the polarization and directionality of light emitted by fibrillar collagen via second harmonic generation to determine structural relationships between collagen in mouse mammary tumor models and the healthy mammary fat pad. In spite of the aberrations in collagen production and degradation that are the hallmarks of tumor stroma, we find that the characteristic angle of SHG scatterers within collagen fibrils, and the spatial extent over which they are appropriately ordered for SHG production, are the same in tumor and healthy collagen. This suggests that the SHG-producing subpopulation of collagen is unaffected by the altered collagen synthesis of the tumor stroma, and protected from its aberrant degradative environment.

©2008 Optical Society of America

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Figures (8)
Fig. 1.
Fig. 1. Enhanced stromal deposition characteristic of many tumors. Masson’s Trichrome staining of TG1-1 tumor cells grown in the mammary fat pad of FVB mice (left) as well as the healthy mammary fat pad of FVB mice (right). Abundant bands of ECM, primarily collagen, are evident throughout the tumor tissue as a blue staining (left), and are largely confined to isolated ducts in the healthy mammary fat pad (blue ring in center of right image). Images are 600 µm across.

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Fig. 2.
Fig. 2. Anti-Collagen I antibody staining of TG1-1 (left) and 4T1 (right) tumor sections, with DAB contrast. Both tumor types show the enhanced ECM deposition characteristic of tumor reactive stroma, evidenced by enhanced dark brown contrast around “islands” of lightly stained tumor cells. Left image is 600 µm across, right is 1.2 mm.

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Fig. 3.
Fig. 3. Experimental Apparatus.

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Fig. 4.
Fig. 4. Radar plot of detected intensity versus analyzer angle. This represents the intensity versus analyzer angle for each of five selected fibrils. In combination with the measured angle of the fibril relative to the laser polarization (vertical in the above graph), Ix, Iy, and hence θ can be extracted from this data for each fibril.

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Fig. 5.
Fig. 5. Measured values of θ in rat tail collagen as well as in different organ systems in the mouse. Error bars are standard deviations. All measurements in mouse organs are statistically significantly different from our measurements in rat (P<0.05), and are not statistically significantly different from each other (p>0.05).

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Fig. 6.
Fig. 6. Top Row: (a) Backward-, and (b) Forward-scattered image of collagen in an acute slice of a TG1-1 mammary adenocarcinoma. Bottom Row: (c) Backward-, and d) Forward-scattered image of collagen in an acute slice of a healthy FVB mammary fat pad. The small dots in the images are calibration beads. Images are 680 microns across.

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Fig. 7.
Fig. 7. The F/B ratio does not vary with apparent diameter of collagen fibrils. A fit straight line slope of zero is within the 95% confidence interval. Note that the PSF has an e-2 radius of 0.67 um. Consequently the stated apparent diameter is a convolution of the Gaussian PSF with the true fibril diameter. However, a deconvolution of the Gaussian PSF with the unknown true distribution (i.e. solid rod, hollow tube, etc.) will rescale the independent variable but will not impart a trend in the data which is not already apparent in the above plots.

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Fig. 8.
Fig. 8. TEM images of collagen in TG1-1 tumor (a), 4T1 tumor (b), and the corresponding healthy FVB and BALB mammary fat pads (c and d, respectively) consists of bundles of rods with a relatively constant characteristic diameter on the order of the ~70 nm predicted by SHG F/B ratio. Collagen fibrils intersecting the image plane transversely appear as streaks (a, b, d) and fibrils intersecting the plane perpendicularly appear as discs (c and d).

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Equations (14)

Equations on this page are rendered with MathJax. Learn more.

P → = χ ( 1 ) * E → + χ ( 2 ) * E ⇀ * E ⇀ + χ ( 3 ) * E ⇀ * E ⇀ * E ⇀
P ⇀ = a s ̂ ( s ̂ · E ⇀ ) 2 + b s ̂ ( E ⇀ · E ⇀ ) + c E ⇀ ( s ̂ · E ⇀ )
I e ∝ ( P ⇀ · e ̂ ) 2 ∝ [ a cos α cos 2 φ + b cos α + c cos ( α − φ ) cos φ ] 2
I y ∝ [ ( a + c ) cos 2 φ + b ] 2
I x ∝ [ c 2 sin 2 φ ] 2
I y I x = [ ( a + c ) cos 2 φ + b ] 2 [ c 2 sin ( 2 φ ) ] 2
a = n − 3 m
c = 2 b = 2 m
n = χ zzz ( 2 ) = N cos 3 θ β
m = χ zxx ( 2 ) = χ xxz ( 2 ) = N 2 cos θ sin 2 θ β
tan 2 θ = 2 cos 2 φ I y I x sin ( 2 φ ) − sin 2 ( φ )
I y ( φ ) = I p [ ρ cos 2 φ + sin 2 φ ] 2
I x ( φ ) = I p [ sin 2 φ ] 2
tan 2 θ = 2 ρ
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