Genetic and histological relationship between pheromone-secreting tissues of the musk gland and skin of juvenile Chinese forest musk deer (<italic style="font-style: italic">Moschus berezovskii </italic>Flerov, 1929)

Long LI; Heran CAO; Jinmeng YANG; Tianqi JIN; Yuxuan MA; Yang WANG; Zhenpeng LI; Yining CHEN; Huihui GAO; Chao ZHU; Tianhao YANG; Yalong DENG; Fangxia YANG; Wuzi DONG

doi:10.1631/jzus.B2200692

Your Location：

Home >

Browse articles >

Genetic and histological relationship between pheromone-secreting tissues of the musk gland and skin of juvenile Chinese forest musk deer (Moschus berezovskii Flerov, 1929)

Scan for full text

Alert me when the article has been cited

Submit

Research Article | Updated：2023-09-13

Genetic and histological relationship between pheromone-secreting tissues of the musk gland and skin of juvenile Chinese forest musk deer (Moschus berezovskii Flerov, 1929)
Genetic and histological relationship between pheromone-secreting tissues of the musk gland and skin of juvenile Chinese forest musk deer (Moschus berezovskii Flerov, 1929)
中国幼年林麝（Moschus berezovskii Flerov, 1929）香腺和皮肤分泌信息素的遗传和组织学关系
Journal of Zhejiang University-SCIENCE B (Biomedicine & Biotechnology) Vol. 24, Issue 9, Pages: 807-822(2023)
Affiliations：

1.College of Animal Science and Technology, Northwest A&F University, Yangling 712100, China
2.College of Forestry, Northwest A&F University, Yangling 712100, China
3.Biology Research Centre of Qin Mountains Wildlife, Northwest A&F University, Yangling 712100, China
Funds：
DOI：10.1631/jzus.B2200692
CLC：
CSTR：

Long LI, Heran CAO, Jinmeng YANG, et al. Genetic and histological relationship between pheromone-secreting tissues of the musk gland and skin of juvenile Chinese forest musk deer (Moschus berezovskii Flerov, 1929). [J]. Journal of Zhejiang University-SCIENCE B (Biomedicine & Biotechnology) 24(9):807-822(2023)
DOI：

Long LI, Heran CAO, Jinmeng YANG, et al. Genetic and histological relationship between pheromone-secreting tissues of the musk gland and skin of juvenile Chinese forest musk deer (Moschus berezovskii Flerov, 1929). [J]. Journal of Zhejiang University-SCIENCE B (Biomedicine & Biotechnology) 24(9):807-822(2023) DOI： 10.1631/jzus.B2200692.

摘要

中国林麝成年雄性的香腺，被认为是一种特殊的皮肤腺体，能够分泌皮脂、脂质和蛋白质等物质进入林麝的香囊。香囊中的物质成熟后称之为麝香，雄性林麝分泌的麝香用来在繁殖季节吸引雌性林麝，且在药用价值和领域标记方面起着重要作用。由于林麝作为国家一级保护动物，组织样品非常珍贵且难以获得，因此中国林麝的麝香腺与皮肤之间的关系仍未被发现。本研究利用组织形态学、RNA测序（RNA-seq）和免疫组化等方法对中国林麝的麝香腺和皮肤进行了检测，并评估了关键调控基因的表达，同时分析皮肤（背部皮肤和腹部皮肤）和香腺的组织结构以确定麝香腺是否来源于皮肤。本研究主要得到如下结果：（1）林麝皮肤和香腺组织共同表达的基因高达88.24%，且Metascap预测分析工具证明麝香腺体中表达的基因具有皮肤组织特异性；（2）免疫化学和分子生物实验证实关键调控基因在皮肤和香腺中均有表达；（3）组织形态学分析结果证实在组织空间结构上香腺和皮肤组织中均含有皮脂腺，推测其原因是麝香中主要成分是脂肪酸（71.55%），且皮脂腺和毛囊作为一个结构单元参与林麝信息素的分泌。

Abstract

Background,2,The musk glands of adult male Chinese forest musk deer (,Moschus berezovskii ,Flerov, 1929) (FMD), which are considered as special skin glands, secrete a mixture of sebum, lipids, and proteins into the musk pod. Together, these components form musk, which plays an important role in attracting females during the breeding season. However, the relationship between the musk glands and skin of Chinese FMD remains undiscovered. Here, the musk gland and skin of Chinese FMD were examined using histological analysis and RNA sequencing (RNA-seq), and the expression of key regulatory genes was evaluated to determine whether the musk gland is derived from the skin.,Methods,2,A comparative analysis of musk gland anatomy between juvenile and adult Chinese FMD was conducted. Then, based on the anatomical structure of the musk gland, skin tissues from the abdomen and back as well as musk gland tissues were obtained from three juvenile FMD. These tissues were used for RNA-seq, hematoxylin-eosin (HE) staining, immunohistochemistry (IHC), western blot (WB), and quantitative real-time polymerase chain reaction (qRT-PCR) experiments.,Results,2,Anatomical analysis showed that only adult male FMD had a complete glandular organ and musk pod, while juvenile FMD did not have any well-developed musk pods. Transcriptomic data revealed that 88.24% of genes were co-expressed in the skin and musk gland tissues. Kyoto Encyclopedia of Genes and Genomes (KEGG) signaling pathway analysis found that the genes co-expressed in the abdomen skin, back skin, and musk gland were enriched in biological development, endocrine system, lipid metabolism, and other pathways. Gene Ontology (GO) enrichment analysis indicated that the genes expressed in these tissues were enriched in biological processes such as multicellular development and cell division. Moreover, the Metascape predictive analysis tool demonstrated that genes expressed in musk glands were skin tissue-specific. qRT-PCR and WB revealed that sex-determining region Y-box protein 9 (,Sox9,),Caveolin-1 (,Cav-1,), and,androgen receptor (,AR,) were expressed in all three tissues, although the expression levels differed among the tissues. According to the IHC results, Sox9 and AR were expressed in the nuclei of sebaceous gland, hair follicle, and musk gland cells, whereas Cav-1 was expressed in the cell membrane.,Conclusions,2,The musk gland of Chinese FMD may be a derivative of skin tissue, and Sox9, Cav-1, and AR may play significant roles in musk gland development.

关键词

林麝信息素麝香腺皮肤组织转录组皮脂腺

Keywords

Forest musk deerPheromonesMusk glandSkin tissuesTranscriptomeSebaceous gland

references

Andrews S, 2014. FastQC a quality control tool for high throughput sequence data. https://www.bioinformatics.babraham.ac.uk/projects/fastqchttps://www.bioinformatics.babraham.ac.uk/projects/fastqc

Barrault C, Garnier J, Pedretti N, et al., 2015. Androgens induce sebaceous differentiation in sebocyte cells expressing a stable functional androgen receptor. J Steroid Biochem Mol Biol, 152:34-44. https://doi.org/10.1016/j.jsbmb.2015.04.005https://doi.org/10.1016/j.jsbmb.2015.04.005

Bastiani M, Liu LB, Hill MM, et al., 2009. MURC/Cavin-4 and cavin family members form tissue-specific caveolar complexes. J Cell Biol, 185(7):1259-1273. https://doi.org/10.1083/jcb.200903053https://doi.org/10.1083/jcb.200903053

Bennett N, Hooper JD, Lee CS, et al., 2009. Androgen receptor and caveolin-1 in prostate cancer. IUBMB Life, 61(10):961-970. https://doi.org/10.1002/iub.244https://doi.org/10.1002/iub.244

Biggs LC, Mikkola ML, 2014. Early inductive events in ectodermal appendage morphogenesis. Semin Cell Dev Biol, 25-26:11-21. https://doi.org/10.1016/j.semcdb.2014.01.007https://doi.org/10.1016/j.semcdb.2014.01.007

Boscher C, Nabi IR, 2012. CAVEOLIN-1: role in cell signaling. In: Jasmin JF, Frank PG, Lisanti MP (Eds.), Caveolins and Caveolae. Advances in Experimental Medicine and Biology, Vol. 729. Springer, New York, p.29-50. https://doi.org/10.1007/978-1-4614-1222-9_3https://doi.org/10.1007/978-1-4614-1222-9_3

Buchfink B, Xie C, Huson DH, 2015. Fast and sensitive protein alignment using DIAMOND. Nat Methods, 12(1):59-60. https://doi.org/10.1038/nmeth.3176https://doi.org/10.1038/nmeth.3176

Chen M, Jie H, Xu ZX, et al., 2018. Isolation, primary culture, and morphological characterization of gland epithelium from forest musk deer (Moschus berezovskii). In Vitro Cell Dev Biol Anim, 54(8):545-548. https://doi.org/10.1007/s11626-018-0268-0https://doi.org/10.1007/s11626-018-0268-0

Codenotti S, Vezzoli M, Poliani PL, et al., 2016. Caveolin-1, Caveolin-2 and Cavin-1 are strong predictors of adipogenic differentiation in human tumors and cell lines of liposarcoma. Eur J Cell Biol, 95(8):252-264. https://doi.org/10.1016/j.ejcb.2016.04.005https://doi.org/10.1016/j.ejcb.2016.04.005

Downie MMT, Guy R, Kealey T, 2004. Advances in sebaceous gland research: potential new approaches to acne management. Int J Cosmet Sci, 26(6):291-311. https://doi.org/10.1111/j.1467-2494.2004.00238.xhttps://doi.org/10.1111/j.1467-2494.2004.00238.x

Duarte MF, Luis C, Baylina P, et al., 2019. Clinical and metabolic implications of obesity in prostate cancer: is testosterone a missing link? Aging Male, 22(4):228-240. https://doi.org/10.1080/13685538.2018.1519695https://doi.org/10.1080/13685538.2018.1519695

Faggi F, Chiarelli N, Colombi M, et al., 2015. Cavin-1 and Caveolin-1 are both required to support cell proliferation, migration and anchorage-independent cell growth in rhabdomyosarcoma. Lab Invest, 95(6):585-602. https://doi.org/10.1038/labinvest.2015.45https://doi.org/10.1038/labinvest.2015.45

Fan MY, Zhang MS, Shi MH, et al., 2018. Sex hormones play roles in determining musk composition during the early stages of musk secretion by musk deer (Moschus berezovskii). Endocr J, 65(11):1111-1120. https://doi.org/10.1507/endocrj.EJ18-0211https://doi.org/10.1507/endocrj.EJ18-0211

Fan ZX, Li WJ, Jin JZ, et al., 2018. The draft genome sequence of forest musk deer (Moschus berezovskii). Gigascience, 7(4):giy038. https://doi.org/10.1093/gigascience/giy038https://doi.org/10.1093/gigascience/giy038

Fridolfsson HN, Roth DM, Insel PA, et al., 2014. Regulation of intracellular signaling and function by caveolin. FASEB J, 28(9):3823-3831. https://doi.org/10.1096/fj.14-252320https://doi.org/10.1096/fj.14-252320

Fu Y, Moore XL, Lee MKS, et al., 2012. Caveolin-1 plays a critical role in the differentiation of monocytes into macrophages. Arterioscler Thromb Vasc Biol, 32(9):e117-e125. https://doi.org/10.1161/atvbaha.112.254151https://doi.org/10.1161/atvbaha.112.254151

Fuchs E, 2016. Epithelial skin biology: three decades of developmental biology, a hundred questions answered and a thousand new ones to address. Curr Top Dev Biol, 116:357-374. https://doi.org/10.1016/bs.ctdb.2015.11.033https://doi.org/10.1016/bs.ctdb.2015.11.033

Haas BJ, Papanicolaou A, Yassour M, et al., 2013. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat Protoc, 8(8):1494-1512. https://doi.org/10.1038/nprot.2013.084https://doi.org/10.1038/nprot.2013.084

Huang SY, Huang GJ, Wu HC, et al., 2018. Ganoderma tsugae inhibits the SREBP-1/AR axis leading to suppression of cell growth and activation of apoptosis in prostate cancer cells. Molecules, 23(10):2539. https://doi.org/10.3390/molecules23102539https://doi.org/10.3390/molecules23102539

Jasmin JF, Yang M, Iacovitti L, et al., 2009. Genetic ablation of caveolin-1 increases neural stem cell proliferation in the subventricular zone (SVZ) of the adult mouse brain. Cell Cycle, 8(23):3978-3983. https://doi.org/10.4161/cc.8.23.10206https://doi.org/10.4161/cc.8.23.10206

Jiang YL, Han XY, Feng NN, et al., 2022. Androgen plays an important role in regulating the synthesis of pheromone in the scent gland of muskrat. J Steroid Biochem Mol Biol, 217:106026. https://doi.org/10.1016/j.jsbmb.2021.106026https://doi.org/10.1016/j.jsbmb.2021.106026

Jo A, Denduluri S, Zhang BS, et al., 2014. The versatile functions of Sox9 in development, stem cells, and human diseases. Genes Dis, 1(2):149-161. https://doi.org/10.1016/j.gendis.2014.09.004https://doi.org/10.1016/j.gendis.2014.09.004

Khurana N, Sikka SC, 2019. Interplay between SOX9, Wnt/β‍-catenin and androgen receptor signaling in castration-resistant prostate cancer. Int J Mol Sci, 20(9):2066. https://doi.org/10.3390/ijms20092066https://doi.org/10.3390/ijms20092066

Li JW, Hassan GS, Williams TM, et al., 2005. Loss of caveolin-1 causes the hyper-proliferation of intestinal crypt stem cells, with increased sensitivity to whole body γ‍-radiation. Cell Cycle, 4(12):1817-1825. https://doi.org/10.4161/cc.4.12.2199https://doi.org/10.4161/cc.4.12.2199

Li RQ, Li YR, Kristiansen K, et al., 2008. SOAP: short oligonucleotide alignment program. Bioinformatics, 24(5):713-714. https://doi.org/10.1093/bioinformatics/btn025https://doi.org/10.1093/bioinformatics/btn025

Lv SQ, Lei ZX, Yan G, et al., 2022. Chemical compositions and pharmacological activities of natural musk (Moschus) and artificial musk: a review. J Ethnopharmacol, 284:114799. https://doi.org/10.1016/j.jep.2021.114799https://doi.org/10.1016/j.jep.2021.114799

Paim FP, Carretero-Pinzón X, Guzmán-Caro DC, et al., 2021. The IUCN Red List of threatened species. https://www.iucnredlist.orghttps://www.iucnredlist.org

Picardo M, Mastrofrancesco A, Bíró T, 2015. Sebaceous gland‒a major player in skin homoeostasis. Exp Dermatol, 24(7):485-486. https://doi.org/10.1111/exd.12720https://doi.org/10.1111/exd.12720

Pretorius E, Africander DJ, Vlok M, et al., 2016. 11-Ketotestosterone and 11-ketodihydrotestosterone in castration resistant prostate cancer: potent androgens which can no longer be ignored. PLoS ONE, 11(7):e0159867. https://doi.org/10.1371/journal.pone.0159867https://doi.org/10.1371/journal.pone.0159867

Quigley CA, de Bellis A, Marschke KB, et al., 1995. Androgen receptor defects: historical, clinical, and molecular perspectives. Endocr Rev, 16(3):271-321. https://doi.org/10.1210/edrv-16-3-271https://doi.org/10.1210/edrv-16-3-271

Rege J, Nakamura Y, Satoh F, et al., 2013. Liquid chromatography-tandem mass spectrometry analysis of human adrenal vein 19-carbon steroids before and after ACTH stimulation. J Clin Endocrinol Metab, 98(3):1182-1188. https://doi.org/10.1210/jc.2012-2912https://doi.org/10.1210/jc.2012-2912

Saga K, 2002. Structure and function of human sweat glands studied with histochemistry and cytochemistry. Prog Histochem Cytochem, 37(4):323-386. https://doi.org/10.1016/s0079-6336(02)80005-5https://doi.org/10.1016/s0079-6336(02)80005-5

Schneider MR, Paus R, 2010. Sebocytes, multifaceted epithelial cells: lipid production and holocrine secretion. Int J Biochem Cell Biol, 42(2):181-185. https://doi.org/10.1016/j.biocel.2009.11.017https://doi.org/10.1016/j.biocel.2009.11.017

Shakhova O, Cheng P, Mishra PJ, et al., 2015. Antagonistic cross-regulation between Sox9 and Sox10 controls an anti-tumorigenic program in melanoma. PLoS Genet, 11(1):e1004877. https://doi.org/10.1371/journal.pgen.1004877https://doi.org/10.1371/journal.pgen.1004877

Shi G, Sohn KC, Li ZJ, et al., 2013. Expression and functional role of Sox9 in human epidermal keratinocytes. PLoS ONE, 8(1):e54355. https://doi.org/10.1371/journal.pone.0054355https://doi.org/10.1371/journal.pone.0054355

Shi G, Wang TT, Quan JH, et al., 2017. Sox9 facilitates proliferation, differentiation and lipogenesis in primary cultured human sebocytes. J Dermatol Sci, 85(1):44-50. https://doi.org/10.1016/j.jdermsci.2016.10.005https://doi.org/10.1016/j.jdermsci.2016.10.005

Shirasu M, Ito S, Itoigawa A, et al., 2020. Key male glandular odorants attracting female ring-tailed lemurs. Curr Biol, 30(11):2131-2138.e4. https://doi.org/10.1016/j.cub.2020.03.037https://doi.org/10.1016/j.cub.2020.03.037

Slessor KN, Winston ML, le Conte Y, 2005. Pheromone communication in the honeybee (Apis mellifera L.). J Chem Ecol, 31(11):2731-2745. https://doi.org/10.1007/s10886-005-7623-9https://doi.org/10.1007/s10886-005-7623-9

Smith KR, Thiboutot DM, 2008. Thematic review series: Skin Lipids. Sebaceous gland lipids: friend or foe? J Lipid Res, 49(2):271-281. https://doi.org/10.1194/jlr.R700015-JLR200https://doi.org/10.1194/jlr.R700015-JLR200

Sokolov VE, Kagan MZ, Vasilieva VS, et al., 1987. Musk deer (Moschus moschiferus): reinvestigation of main lipid components from preputial gland secretion. J Chem Ecol, 13(1):71-83. https://doi.org/10.1007/bf01020352https://doi.org/10.1007/bf01020352

Sotgia F, Williams TM, Cohen AW, et al., 2005. Caveolin-1-deficient mice have an increased mammary stem cell population with upregulation of Wnt/β-catenin signaling. Cell Cycle, 4(12):1808-1816. https://doi.org/10.4161/cc.4.12.2198https://doi.org/10.4161/cc.4.12.2198

Sotiropoulou PA, Blanpain C, 2012. Development and homeostasis of the skin epidermis. Cold Spring Harb Perspect Biol, 4(7):a008383. https://doi.org/10.1101/cshperspect.a008383https://doi.org/10.1101/cshperspect.a008383

Storbeck KH, Bloem LM, Africander D, et al., 2013. 11β- Hydroxydihydrotestosterone and 11-ketodihydrotestosterone, novel C19 steroids with androgenic activity: a putative role in castration resistant prostate cancer? Mol Cell Endocrinol, 377(1-2):135-146. https://doi.org/10.1016/j.mce.2013.07.006https://doi.org/10.1016/j.mce.2013.07.006

Su RN, Dalai M, Luvsantseren B, et al., 2022. Comparative study of the function and structure of the gut microbiota in Siberian musk deer and Forest musk deer. Appl Microbiol Biotechnol, 106(19-20):6799-6817. https://doi.org/10.1007/s00253-022-12158-9https://doi.org/10.1007/s00253-022-12158-9

Tamai O, Oka N, Kikuchi T, et al., 2001. Caveolae in mesangial cells and caveolin expression in mesangial proliferative glomerulonephritis. Kidney Int, 59(2):471-480. https://doi.org/10.1046/j.1523-1755.2001.059002471.xhttps://doi.org/10.1046/j.1523-1755.2001.059002471.x

Thody AJ, Shuster S, 1989. Control and function of sebaceous glands. Physiol Rev, 69(2):383-416. https://doi.org/10.1152/physrev.1989.69.2.383https://doi.org/10.1152/physrev.1989.69.2.383

Varendi H, Porter RH, 2001. Breast odour as the only maternal stimulus elicits crawling towards the odour source. Acta Paediatr, 90(4):372-375.

Vidal VPI, Ortonne N, Schedl A, 2008. SOX9 expression is a general marker of basal cell carcinoma and adnexal-related neoplasms. J Cutan Pathol, 35(4):373-379. https://doi.org/10.1111/j.1600-0560.2007.00815.xhttps://doi.org/10.1111/j.1600-0560.2007.00815.x

Yang JM, Peng GF, Shu F, et al., 2021. Characteristics of steroidogenesis-related factors in the musk gland of Chinese forest musk deer (Moschus berezovskii). J Steroid Biochem Mol Biol, 212:105916. https://doi.org/10.1016/j.jsbmb.2021.105916https://doi.org/10.1016/j.jsbmb.2021.105916

Yang RH, Wang JR, Zhou ZH, et al., 2019. Role of caveolin-1 in epidermal stem cells during burn wound healing in rats. Dev Biol, 445(2):271-279. https://doi.org/10.1016/j.ydbio.2018.11.015https://doi.org/10.1016/j.ydbio.2018.11.015

Zhang TX, Zhang MS, Shi MH, et al., 2021. Musk secretion in muskrats (Ondatra zibethicus L.): association with lipid and cholesterol metabolism-related pathways. Biocell, 45(2):281-306. https://doi.org/10.32604/biocell.2021.010277https://doi.org/10.32604/biocell.2021.010277

Zhao KL, Liu Y, Zhang XY, et al., 2011. Detection and characterization of antibiotic-resistance genes in Arcanobacterium pyogenes strains from abscesses of forest musk deer. J Med Microbiol, 60(12):1820-1826. https://doi.org/10.1099/jmm.0.033332-0https://doi.org/10.1099/jmm.0.033332-0

Zhou YY, Zhou B, Pache L, et al., 2019. Metascape provides a biologist-oriented resource for the analysis of systems-level datasets. Nat Commun, 10:1523. https://doi.org/10.1038/s41467-019-09234-6https://doi.org/10.1038/s41467-019-09234-6

Zouboulis CC, Baron JM, Böhm M, et al., 2008. Frontiers in sebaceous gland biology and pathology. Exp Dermatol, 17(6):542-551. https://doi.org/10.1111/j.1600-0625.2008.00725.xhttps://doi.org/10.1111/j.1600-0625.2008.00725.x

Views

Downloads

CSCD

Tools

Publicity Resources

Spatial transcriptome analysis of long non-coding RNAs reveals tissue specificity and functional roles in cancer

De-novo characterization of the soft-shelled turtle Pelodiscus sinensis transcriptome using Illumina RNA-Seq technology#

Global impact of RNA splicing on transcriptome remodeling in the heart

Related Author

No data

Related Institution

College of Bioinformatics Science and Technology, Harbin Medical University

Key Laboratory of Tropical Translational Medicine of Ministry of Education, College of Biomedical Information and Engineering, Hainan Women and Children’s Medical Center, Hainan Medical University

Zhejiang Provincial Top Key Discipline of Modern Microbiology and Application, College of Biological and Environmental Sciences, Zhejiang Wanli University

Henan Provincial Bureau of Animal Husbandry

Molecular Biology Institutes, University of Los Angeles

Address：Journal of Zhejiang University-SCIENCE, 38 Zheda Road, Hangzhou, China Postal code：310027
Tel：+86-571-87952783 Email：cjzhang@zju.edu.cn
Technical support is provided by Beijing Founder electronics co., LTD 京ICP备09064830号-19 京公网安备11010802024621
It is recommended to read the content of this site in Chrome&IE9+. Please switch to extreme mode in browser 360.
Cookies We use cookies to help provide and enhance our service and tailor content. By continuing, you agree to the use of cookies.

⁰

Genetic and histological relationship between pheromone-secreting tissues of the musk gland and skin of juvenile Chinese forest musk deer (Moschus berezovskii Flerov, 1929)

Genetic and histological relationship between pheromone-secreting tissues of the musk gland and skin of juvenile Chinese forest musk deer (Moschus berezovskii Flerov, 1929)

DOI：10.1631/jzus.B2200692

摘要

Abstract

关键词

Keywords

references