Application Progress of Tissue Clearing Three-Dimensional Imaging Technology in Ovarian Tissue

doi:10.12280/gjfckx.20220292

Abstract

Abstract:

The ovaries are important organs of the mammalian reproductive system, and the understanding of the ovaries is mostly at the two-dimensional level. The rapid development of tissue clearing three-dimensional imaging technology provides an advanced platform for three-dimensional D visualization of the ovaries, which not only can be used to comprehensively image the normal and pathological ovarian tissues through tissue clearing and optical imaging microscopy techniques and explore ovarian tissue and its relationship with the vasculature and nervous system from the cellular or subcellular unit level, but also reveal the spatial relationship and structural characteristics of ovarian tissue. This technique can also analyze the three-dimensional structure and growth pattern of ovarian tumors, and study the density, integrity and morphological heterogeneity of the vasculature and nervous system, providing direction for the treatment and prognosis of ovarian tumors. In this article, we review the application progress of tissue clearing three-dimensional imaging technology in mammalian ovarian tissue, with a view to gaining a deeper understanding of ovarian tissue.

Key words: Ovary, Ovarian neoplasms, Tissue clearing technology, Imaging, three-dimensional, Diagnostic imaging, Microscopy, Optics and photonics

CHEN Ying, HUANG Jin-zhi, WU Ke-feng, LI Qian. Application Progress of Tissue Clearing Three-Dimensional Imaging Technology in Ovarian Tissue[J]. Journal of International Obstetrics and Gynecology, 2022, 49(5): 492-496.

Figures/Tables 1

References 29

[1]	Tian T, Yang Z, Li X. Tissue clearing technique: Recent progress and biomedical applications[J]. J Anat, 2021, 238(2):489-507. doi: 10.1111/joa.13309. doi: 10.1111/joa.13309
[2]	Gómez-Gaviro MV, Sanderson D, Ripoll J, et al. Biomedical Applications of Tissue Clearing and Three-Dimensional Imaging in Health and Disease[J]. iScience, 2020, 23(8):101432. doi: 10.1016/j.isci.2020.101432. doi: 10.1016/j.isci.2020.101432
[3]	Zhao S, Todorov MI, Cai R, et al. Cellular and Molecular Probing of Intact Human Organs[J]. Cell, 2020, 180(4):796-812.e19. doi: 10.1016/j.cell.2020.01.030. doi: S0092-8674(20)30111-2 pmid: 32059778
[4]	Cipollari S, Jamshidi N, Du L, et al. Tissue clearing techniques for three-dimensional optical imaging of intact human prostate and correlations with multi-parametric MRI[J]. Prostate, 2021, 81(9):521-529. doi: 10.1002/pros.24129. doi: 10.1002/pros.24129 pmid: 33876838
[5]	Almagro J, Messal HA, Zaw Thin M, et al. Tissue clearing to examine tumour complexity in three dimensions[J]. Nat Rev Cancer, 2021, 21(11):718-730. doi: 10.1038/s41568-021-00382-w. doi: 10.1038/s41568-021-00382-w
[6]	Matsumoto K, Mitani TT, Horiguchi SA, et al. Advanced CUBIC tissue clearing for whole-organ cell profiling[J]. Nat Protoc, 2019, 14(12):3506-3537. doi: 10.1038/s41596-019-0240-9. doi: 10.1038/s41596-019-0240-9 pmid: 31748753
[7]	Hillman E, Voleti V, Li W, et al. Light-Sheet Microscopy in Neuroscience[J]. Annu Rev Neurosci, 2019, 42:295-313. doi: 10.1146/annurev-neuro-070918-050357. doi: 10.1146/annurev-neuro-070918-050357 pmid: 31283896
[8]	Jafree DJ, Long DA, Scambler PJ, et al. Tissue Clearing and Deep Imaging of the Kidney Using Confocal and Two-Photon Microscopy[J]. Methods Mol Biol, 2020, 2067:103-126. doi: 10.1007/978-1-4939-9841-8_8. doi: 10.1007/978-1-4939-9841-8_8 pmid: 31701448
[9]	Feuchtinger A, Walch A, Dobosz M. Deep tissue imaging: a review from a preclinical cancer research perspective[J]. Histochem Cell Biol, 2016, 146(6):781-806. doi: 10.1007/s00418-016-1495-7. doi: 10.1007/s00418-016-1495-7 pmid: 27704211
[10]	Sabdyusheva Litschauer I, Becker K, Saghafi S, et al. 3D histopathology of human tumours by fast clearing and ultramicroscopy[J]. Sci Rep, 10(1):17619. doi: 10.1038/s41598-020-71737-w. doi: 10.1038/s41598-020-71737-w
[11]	Hong SM, Jung D, Kiemen A, et al. Three-dimensional visualization of cleared human pancreas cancer reveals that sustained epithelial-to-mesenchymal transition is not required for venous invasion[J]. Mod Pathol, 2020, 33(4):639-647. doi: 10.1038/s41379-019-0409-3. doi: 10.1038/s41379-019-0409-3
[12]	Zucker RM, Jeffay SC. Confocal laser scanning microscopy of whole mouse ovaries: excellent morphology, apoptosis detection, and spectroscopy[J]. Cytometry A, 2006, 69(8):930-939. doi: 10.1002/cyto.a.20315. doi: 10.1002/cyto.a.20315
[13]	Svingen T, François M, Wilhelm D, et al. Three-dimensional imaging of Prox1-EGFP transgenic mouse gonads reveals divergent modes of lymphangiogenesis in the testis and ovary[J]. PLoS One, 2012, 7(12):e52620. doi: 10.1371/journal.pone.0052620. doi: 10.1371/journal.pone.0052620
[14]	Faire M, Skillern A, Arora R, et al. Follicle dynamics and global organization in the intact mouse ovary[J]. Dev Biol, 2015, 403(1):69-79. doi: 10.1016/j.ydbio.2015.04.006. doi: 10.1016/j.ydbio.2015.04.006 pmid: 25889274
[15]	Soygur B, Jaszczak RG, Fries A, et al. Intercellular bridges coordinate the transition from pluripotency to meiosis in mouse fetal oocytes[J]. Sci Adv, 2021, 7(15):eabc6747. doi: 10.1126/sciadv.abc6747. doi: 10.1126/sciadv.abc6747
[16]	Tanaka N, Kanatani S, Tomer R, et al. Whole-tissue biopsy phenotyping of three-dimensional tumours reveals patterns of cancer heterogeneity[J]. Nat Biomed Eng, 2017, 1(10):796-806. doi: 10.1038/s41551-017-0139-0. doi: 10.1038/s41551-017-0139-0 pmid: 31015588
[17]	Masselink W, Reumann D, Murawala P, et al. Broad applicability of a streamlined ethyl cinnamate-based clearing procedure[J]. Development, 2019, 146(3):dev166884. doi: 10.1242/dev.166884. doi: 10.1242/dev.166884
[18]	Kagami K, Shinmyo Y, Ono M, et al. Three-dimensional evaluation of murine ovarian follicles using a modified CUBIC tissue clearing method[J]. Reprod Biol Endocrinol, 2018, 16(1):72. doi: 10.1186/s12958-018-0381-7. doi: 10.1186/s12958-018-0381-7
[19]	Tong X, Liu Y, Xu X, et al. Ovarian Innervation Coupling With Vascularity: The Role of Electro-Acupuncture in Follicular Maturation in a Rat Model of Polycystic Ovary Syndrome[J]. Front Physiol, 2020, 11:474. doi: 10.3389/fphys.2020.00474. doi: 10.3389/fphys.2020.00474 pmid: 32547407
[20]	Boateng R, Boechat N, Henrich PP, et al. Whole Ovary Immunofluorescence, Clearing, and Multiphoton Microscopy for Quantitative 3D Analysis of the Developing Ovarian Reserve in Mouse[J]. J Vis Exp, 2021, 175:62972. doi: 10.3791/62972. doi: 10.3791/62972
[21]	Malki S, Tharp ME, Bortvin A. A Whole-Mount Approach for Accurate Quantitative and Spatial Assessment of Fetal Oocyte Dynamics in Mice[J]. Biol Reprod, 2015, 93(5):113. doi: 10.1095/biolreprod.115.132118. doi: 10.1095/biolreprod.115.132118 pmid: 26423126
[22]	Rinaldi VD, Bloom JC, Schimenti JC. Whole Mount Immunofluorescence and Follicle Quantification of Cultured Mouse Ovaries[J]. J Vis Exp, 2018, 135:57593. doi: 10.3791/57593. doi: 10.3791/57593
[23]	Feng Y, Cui P, Lu X, et al. CLARITY reveals dynamics of ovarian follicular architecture and vasculature in three-dimensions[J]. Sci Rep, 2017, 7:44810. doi: 10.1038/srep44810. doi: 10.1038/srep44810 pmid: 28333125
[24]	Hu W, Tamadon A, Hsueh A, et al. Three-dimensional Reconstruction of the Vascular Architecture of the Passive CLARITY-cleared Mouse Ovary[J]. J Vis Exp, 2017, 130:56141. doi: 10.3791/56141. doi: 10.3791/56141
[25]	Ma T, Cui P, Tong X, et al. Endogenous Ovarian Angiogenesis in Polycystic Ovary Syndrome-Like Rats Induced by Low-Frequency Electro-Acupuncture: The CLARITY Three-Dimensional Approach[J]. Int J Mol Sci, 2018, 19(11):3500. doi: 10.3390/ijms19113500. doi: 10.3390/ijms19113500
[26]	Oren R, Fellus-Alyagor L, Addadi Y, et al. Whole Organ Blood and Lymphatic Vessels Imaging (WOBLI)[J]. Sci Rep, 2018, 8(1):1412. doi: 10.1038/s41598-018-19663-w. doi: 10.1038/s41598-018-19663-w pmid: 29362484
[27]	McKey J, Cameron LA, Lewis D, et al. Combined iDISCO and CUBIC tissue clearing and lightsheet microscopy for in toto analysis of the adult mouse ovary?[J]. Biol Reprod, 2020, 102(5):1080-1089. doi: 10.1093/biolre/ioaa012. doi: 10.1093/biolre/ioaa012
[28]	Lesage M, Thomas M, Bugeon J, et al. C-ECi: a CUBIC-ECi combined clearing method for three-dimensional follicular content analysis in the fish ovary?[J]. Biol Reprod, 2020, 103(5):1099-1109. doi: 10.1093/biolre/ioaa142. doi: 10.1093/biolre/ioaa142 pmid: 32776144
[29]	Fiorentino G, Parrilli A, Garagna S, et al. Three-Dimensional Micro-Computed Tomography of the Adult Mouse Ovary[J]. Front Cell Dev Biol, 2020, 8:566152. doi: 10.3389/fcell.2020.566152. doi: 10.3389/fcell.2020.566152

分类	作者	发表时间	透明化方法	卵巢来源	研究内容	显微镜类型
有机溶剂型	Zucker等^[12]	2006年	BABB	小鼠卵巢	可视化卵巢形态和细胞凋亡	共聚焦显微镜
	Svingen等^[13]	2012年	BABB	小鼠卵巢	卵巢中淋巴管生成	共聚焦显微镜、荧光显微镜
	Faire等^[14]	2015年	BABB	小鼠卵巢	辨别卵巢卵泡的生长状态,提供更高通量的卵泡计数方法	共聚焦显微镜
	Soygur等^[15]	2021年	BABB	小鼠卵巢	小鼠胎儿完整卵巢中的减数分裂起始	共聚焦显微镜
	Tanaka等^[16]	2017年	iDISCO	人类卵巢癌	血管半径和CD34密度方差以及药物反应性之间的相关性	光片显微镜、荧光显微镜
	Masselink等^[17]	2019年	2Eci	果蝇卵巢	标记卵泡成熟的整个过程,从生发干细胞到减数分裂和卵子形成	光片显微镜、共聚焦显微镜
亲水溶剂型	Kagami等^[18]	2018年	CUBIC	小鼠卵巢	单个卵母细胞的三维定位,进一步明确卵泡的三维结构	共聚焦显微镜、光片显微镜
	Tong等^[19]	2020年	CUBIC	小鼠卵巢	确定神经支配在卵泡生成和血管形成中的作用	光片显微镜
	Soygur等^[15]	2021年	Scale CUBIC	小鼠卵巢	完整小鼠胎儿卵巢中的减数分裂起始	共聚焦显微镜
	Boateng等^[20]	2021年	ScaleS和CUBIC	小鼠卵巢	全卵巢的卵母细胞数量	多光子显微镜
	Malki等^[21]	2015年	ScaleA2	小鼠卵巢	对完整卵巢中的生殖细胞进行自动检测和计数	共聚焦显微镜
	Rinaldi等^[22]	2018年	ScaleS	小鼠卵巢	卵母细胞定量	共聚焦显微镜
主动型	Feng等^[23]	2017年	CLARITY	小鼠卵巢	卵泡动力学、卵泡发生与卵巢脉管系统之间的关系	共聚焦显微镜
	Hu等^[24]	2017年	CLARITY	小鼠卵巢	卵巢脉管的三维连接和结构,以及卵泡和脉管之间的三维结构关系	共聚焦显微镜
	Ma等^[25]	2018年	CLARITY	大鼠卵巢	分析不同类型卵泡的数量及其与局部脉管系统的关系	共聚焦显微镜
组合型	Oren等^[26]	2018年	WOBLI（CLARITY 和ScaleA2）	小鼠卵巢	分析并生成淋巴和脉管系统的结构信息	光片显微镜
	McKey等^[27]	2020年	iDISCO和CUBIC	小鼠卵巢	对发育的各个阶段的卵泡进行了定性评估,并研究包括脉管和神经网络在内的卵巢外成分的完整性	光片显微镜、共聚焦显微镜
	Lesage等^[28]	2020年	CUBIC-ECi	青鳉和鳟鱼的卵巢	鱼类卵巢中卵泡的定量	共聚焦显微镜

分类	作者	发表时间	透明化方法	卵巢来源	研究内容	显微镜类型
有机溶剂型	Zucker等^[12]	2006年	BABB	小鼠卵巢	可视化卵巢形态和细胞凋亡	共聚焦显微镜
	Svingen等^[13]	2012年	BABB	小鼠卵巢	卵巢中淋巴管生成	共聚焦显微镜、荧光显微镜
	Faire等^[14]	2015年	BABB	小鼠卵巢	辨别卵巢卵泡的生长状态,提供更高通量的卵泡计数方法	共聚焦显微镜
	Soygur等^[15]	2021年	BABB	小鼠卵巢	小鼠胎儿完整卵巢中的减数分裂起始	共聚焦显微镜
	Tanaka等^[16]	2017年	iDISCO	人类卵巢癌	血管半径和CD34密度方差以及药物反应性之间的相关性	光片显微镜、荧光显微镜
	Masselink等^[17]	2019年	2Eci	果蝇卵巢	标记卵泡成熟的整个过程,从生发干细胞到减数分裂和卵子形成	光片显微镜、共聚焦显微镜
亲水溶剂型	Kagami等^[18]	2018年	CUBIC	小鼠卵巢	单个卵母细胞的三维定位,进一步明确卵泡的三维结构	共聚焦显微镜、光片显微镜
	Tong等^[19]	2020年	CUBIC	小鼠卵巢	确定神经支配在卵泡生成和血管形成中的作用	光片显微镜
	Soygur等^[15]	2021年	Scale CUBIC	小鼠卵巢	完整小鼠胎儿卵巢中的减数分裂起始	共聚焦显微镜
	Boateng等^[20]	2021年	ScaleS和CUBIC	小鼠卵巢	全卵巢的卵母细胞数量	多光子显微镜
	Malki等^[21]	2015年	ScaleA2	小鼠卵巢	对完整卵巢中的生殖细胞进行自动检测和计数	共聚焦显微镜
	Rinaldi等^[22]	2018年	ScaleS	小鼠卵巢	卵母细胞定量	共聚焦显微镜
主动型	Feng等^[23]	2017年	CLARITY	小鼠卵巢	卵泡动力学、卵泡发生与卵巢脉管系统之间的关系	共聚焦显微镜
	Hu等^[24]	2017年	CLARITY	小鼠卵巢	卵巢脉管的三维连接和结构,以及卵泡和脉管之间的三维结构关系	共聚焦显微镜
	Ma等^[25]	2018年	CLARITY	大鼠卵巢	分析不同类型卵泡的数量及其与局部脉管系统的关系	共聚焦显微镜
组合型	Oren等^[26]	2018年	WOBLI（CLARITY 和ScaleA2）	小鼠卵巢	分析并生成淋巴和脉管系统的结构信息	光片显微镜
	McKey等^[27]	2020年	iDISCO和CUBIC	小鼠卵巢	对发育的各个阶段的卵泡进行了定性评估,并研究包括脉管和神经网络在内的卵巢外成分的完整性	光片显微镜、共聚焦显微镜
	Lesage等^[28]	2020年	CUBIC-ECi	青鳉和鳟鱼的卵巢	鱼类卵巢中卵泡的定量	共聚焦显微镜