Dissecting Mammalian Spermatogenesis Using Spatial Transcriptomics
Posted on: 7 January 2021
Preprint posted on 17 October 2020
Article now published in Cell Reports at http://dx.doi.org/10.1016/j.celrep.2021.109915
I told my supervisor that we need space - in my experiments. Using spatial transcriptomics to dissect mammalian spermatogenesis.
Selected by Martin Estermann
Categories: bioinformatics, cell biology, developmental biology, genetics, genomics, immunology, molecular biology, physiology
Background:
One of the main testicular functions is to produce male gametes (sperm cells), which are crucial for sexual reproduction. Two main compartments are distinguishable in the testis, the seminiferous tubules, fine coiled tubular structures where spermatogenesis takes place, and the peritubular space. The tubules contain layers of germ cells, that develop into sperm cells (also known as spermatozoa), in close association with Sertoli cells. Steroidogenic Leydig cells, macrophages and other interstitial cells are located in the space between the tubules.
Spermatogenesis is a controlled process that begins postnatally and culminates with the production of the first sperm at the onset of sexual maturity. In mice, the seminiferous tubules periodically cycle through 12 stages (I-XII) that are defined by the combination of germ cells present. Recently, testicular single-cell RNA sequencing (scRNA-seq) studies showed that not only the germ cells are stage specific but other cells like Sertoli cells also vary from stage to stage.
scRNA-seq introduced a fundamental change in the focus of the research and gene expression. Instead of using the whole organ as a research unit, it is partitioned to the smallest structural and functional unit, the single cell. One of the main issues concerning single-cell technologies is that spatial and tissue organization information is lost when generating a single-cell suspension. Spatial transcriptomics was developed as a new methodology to overcome this problem. Briefly, frozen tissue sections are placed on a slide containing barcoded spots (bead array) that provide a specific spatial orientation. The cells in the tissue sections are permeabilized, allowing mRNA to be bound to the most proximal barcode, followed by cDNA synthesis and sequencing. The barcode sequence associates each transcript with a spatial position, assigning mRNA expression to different tissue regions (Fig. 1).
The authors used spatial transcriptomics in mouse and human testis to develop a spatial transcriptome atlas for mammalian spermatogenesis, being able to assign information of cell type, seminiferous tubule, and stage to each bead with high accuracy. Furthermore, the authors provided evidence for the diagnostic value of this technology by characterizing the testicular disorganization in a diabetic mouse model.
Fig 1. Spatial transcriptomics workflow. (Preprint Fig. 1A and B).
Key findings
1) Spatial transcriptome atlas for mouse spermatogenesis
Mouse 10 um frozen testicular sections were captured into a slide-seq array and subjected to spatial transcriptomics, detecting around 30,000 beads (“cells”) per array. The different beads were assigned with a cell type and were mapped into the array, which reflected the structure of the testicular seminiferous tubules (Fig. 2A). After the cell type assignment, the array was partitioned into the distinctive seminiferous tubules (Fig. 2B) and classified into one of the four major stages of seminiferous tubules using known stage-dependent markers: stages I-III, IV-VI, VII-VIII or IX-XII (Fig. 2C).
Stage-specific Sertoli and germ cells are well characterized in the literature, but the cells in the testicular interstitium and the peritubular space remain largely unexplored. The authors were able to identify transcriptomic signatures of stage specific Leydig (steroidogenic) cells (Fig. 2D) and macrophages (Fig. 2E) never reported before.
Fig 2. Mouse testicular spatial transcriptomics. (A) Spatial mapping of testicular cell types in mouse section. ES: elongated/elongating spermatid, RS: round spermatid, SPC: spermatocyte, SPG: spermatogonium. (B) Digital segmentation of the seminiferous tubules. (C) Spatial mapping of the four stage clusters. (D) Schematic representation of the spatial localization and marker genes for each stage dependent Leydig cell. (E) Schematic representation of the spatial localization and marker genes for each stage dependent macrophage. (Preprint Fig. 1C, 1F, 1H, 3A, 3C and 3D).
2) Spatial transcriptome atlas for human spermatogenesis
The next challenge was to apply this pipeline to human testicular samples, spatially mapping human testicular cell types (Fig 3A). In order to validate these results, the authors used the Human Protein Atlas database to corroborate the expression pattern of different spermatogonia genes into the seminiferous tubules (Fig. 3B). This resulted in around 74% of match, with the remaining 26% not being present in the protein database or showing non-specific immunostaining. An example of four genes with differential expression from the lumen (left) to the basement membrane (right) can be found in Fig. 3B.
Recently, human testicular single-cell RNA sequencing revealed 5 transcriptional states of human spermatogonia (0-4). Using the described expression markers, two different microenvironments of spermatogonia coexist in the same seminiferous tubule, one containing mostly state 0 spermatogonia (naïve/stem cell) and the other containing states 1-4 and the remaining state 0 (Fig. 3C).
Fig 3. Human testicular spatial transcriptomics. (A) Spatial mapping of testicular cell types in human section. ES: elongated/elongating spermatid, RS: round spermatid, SPC: spermatocyte, SPG: spermatogonium. (B) Spatial expression patterns of the genes ACTRT3, ACRBP, CLDN11 and GSTA1 from the spatial transcriptomic atlas and the human protein atlas. (C) Spatial mapping of the five human spermatogonia germ cells. (Preprint Fig. 4 A, B and D).
3) Testicular spatial transcriptomics in diabetes-induced testicular injuries
Several reports indicate that diabetes mellitus results in disturbances in the male reproductive system, but the exact mechanism is still unknown. To evaluate if the slide-seq workflow could be applied to study testicular diseases, leptin-deficient diabetic mice (ob/ob) testis were compared with wild type testis (WT), using spatial transcriptomics (Fig. 4A). Differential expression analysis identified a downregulation of elongating/elongated spermatids genes such as Smcp and Odf1 (Fig. 4B). This is consistent with the loss of elongated spermatids in ob/ob testes. Furthermore, mitochondrial genes were elevated, a condition associated with mitochondrial dysfunction and mtDNA damage.
A disorganization in the seminiferous tubules structure was also detected in the ob/ob mice testes. To quantify these changes, a purity score was generated, taking into account the spatial mixing of the elongated spermatids beads with beads of other cell types (Fig. 4C). In the wild type mice, the elongated spermatids beads clustered in the centre of the seminiferous tubule, showing a high purity score (0.63). In contrast, in ob/ob seminiferous tubules, the elongated spermatids beads were likely to make contacts with beads of other cell types, reflecting a lower purity score (0.44) and a structural disorganization.
Fig 4. Diabetes causes disruption in the testicular seminiferous tubules. (A) Spatial mapping of the testicular cell types in wild type (WT) and leptin-deficient diabetic (ob/ob) samples. ES: elongated/elongating spermatid, RS: round spermatid, SPC: spermatocyte, SPG: spermatogonium. (B) Spatial expression pattern of Smcp and Odf1 genes in a representative WT and ob/ob seminiferous tubule. (C) Elongated spermatid purity score for each Slide-seq bead in a representative WT and ob/ob seminiferous tubule. (Preprint Fig. 5A, C and S11).
Why I choose this paper:
One of the main issues around single-cell technologies is that spatial and tissue organization information is lost when generating a single-cell suspension. Spatial transcriptomics was developed as a new methodology to overcome this problem. This study demonstrated the utility of this emerging technique by characterizing testicular spermatogenesis in mouse and human tissue with high accuracy. Furthermore, the authors provided evidence for the diagnostic value of this technology by characterizing the testicular disorganization in a diabetic mouse model. The spatial atlases generated can be useful to identify cellular and molecular changes associated with different diseases.
The used protocol can easily be adapted to other tissues, animal models or human samples and provides the first workflow that could be used in the clinic. Tissue biopsies from testicular cancer, infertility or differences of sex development (DSDs) could potentially be subjected to spatial transcriptomics in the near future.
Future directions / questions for the authors:
- Sertoli and germ cells grow in really close association, how hard was it for you to differentiate both cell types? How often did you find Sertoli and sperm cells transcripts in the same bead?
- In your opinion, what would be the next step required to bring spatial transcriptomics into a clinical setting?
doi: https://doi.org/10.1242/prelights.26837
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This 2024 Hypothalamus GRC (Gordon Research Conference) preList offers an overview of cutting-edge research focused on the hypothalamus, a critical brain region involved in regulating homeostasis, behavior, and neuroendocrine functions. The studies included cover a range of topics, including neural circuits, molecular mechanisms, and the role of the hypothalamus in health and disease. This collection highlights some of the latest advances in understanding hypothalamic function, with potential implications for treating disorders such as obesity, stress, and metabolic diseases.
| List by | Nathalie Krauth |
BSCB-Biochemical Society 2024 Cell Migration meeting
This preList features preprints that were discussed and presented during the BSCB-Biochemical Society 2024 Cell Migration meeting in Birmingham, UK in April 2024. Kindly put together by Sara Morais da Silva, Reviews Editor at Journal of Cell Science.
| List by | Reinier Prosee |
‘In preprints’ from Development 2022-2023
A list of the preprints featured in Development's 'In preprints' articles between 2022-2023
| List by | Alex Eve, Katherine Brown |
CSHL 87th Symposium: Stem Cells
Preprints mentioned by speakers at the #CSHLsymp23
| List by | Alex Eve |
9th International Symposium on the Biology of Vertebrate Sex Determination
This preList contains preprints discussed during the 9th International Symposium on the Biology of Vertebrate Sex Determination. This conference was held in Kona, Hawaii from April 17th to 21st 2023.
| List by | Martin Estermann |
Alumni picks – preLights 5th Birthday
This preList contains preprints that were picked and highlighted by preLights Alumni - an initiative that was set up to mark preLights 5th birthday. More entries will follow throughout February and March 2023.
| List by | Sergio Menchero et al. |
CellBio 2022 – An ASCB/EMBO Meeting
This preLists features preprints that were discussed and presented during the CellBio 2022 meeting in Washington, DC in December 2022.
| List by | Nadja Hümpfer et al. |
EMBL Synthetic Morphogenesis: From Gene Circuits to Tissue Architecture (2021)
A list of preprints mentioned at the #EESmorphoG virtual meeting in 2021.
| List by | Alex Eve |
FENS 2020
A collection of preprints presented during the virtual meeting of the Federation of European Neuroscience Societies (FENS) in 2020
| List by | Ana Dorrego-Rivas |
ECFG15 – Fungal biology
Preprints presented at 15th European Conference on Fungal Genetics 17-20 February 2020 Rome
| List by | Hiral Shah |
ASCB EMBO Annual Meeting 2019
A collection of preprints presented at the 2019 ASCB EMBO Meeting in Washington, DC (December 7-11)
| List by | Madhuja Samaddar et al. |
Lung Disease and Regeneration
This preprint list compiles highlights from the field of lung biology.
| List by | Rob Hynds |
MitoList
This list of preprints is focused on work expanding our knowledge on mitochondria in any organism, tissue or cell type, from the normal biology to the pathology.
| List by | Sandra Franco Iborra |
Also in the physiology category:
Fibroblasts
The advances in fibroblast biology preList explores the recent discoveries and preprints of the fibroblast world. Get ready to immerse yourself with this list created for fibroblasts aficionados and lovers, and beyond. Here, my goal is to include preprints of fibroblast biology, heterogeneity, fate, extracellular matrix, behavior, topography, single-cell atlases, spatial transcriptomics, and their matrix!
| List by | Osvaldo Contreras |
FENS 2020
A collection of preprints presented during the virtual meeting of the Federation of European Neuroscience Societies (FENS) in 2020
| List by | Ana Dorrego-Rivas |
TAGC 2020
Preprints recently presented at the virtual Allied Genetics Conference, April 22-26, 2020. #TAGC20
| List by | Maiko Kitaoka et al. |
Autophagy
Preprints on autophagy and lysosomal degradation and its role in neurodegeneration and disease. Includes molecular mechanisms, upstream signalling and regulation as well as studies on pharmaceutical interventions to upregulate the process.
| List by | Sandra Malmgren Hill |
Cellular metabolism
A curated list of preprints related to cellular metabolism at Biorxiv by Pablo Ranea Robles from the Prelights community. Special interest on lipid metabolism, peroxisomes and mitochondria.
| List by | Pablo Ranea Robles |