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Article: Male-pattern hair loss: Comprehensive identification of the associated genes as a basis for understanding pathophysiology

Henne, Sabrina K. / Nöthen, Markus M. / Heilmann-Heimbach, Stefanie

2023 Volume 35, Issue 1, Page(s) 3

Language	German
Document type	Article
ZDB-ID	1083376-6
ISSN	0936-5931
Database	Current Contents Medicine

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Article ; Online: Genetic prediction of male pattern baldness based on large independent datasets.

Chen, Yan / Hysi, Pirro / Maj, Carlo / Heilmann-Heimbach, Stefanie / Spector, Timothy D / Liu, Fan / Kayser, Manfred

European journal of human genetics : EJHG

2022 Volume 31, Issue 3, Page(s) 321–328

Abstract: Genetic prediction of male pattern baldness (MPB) is important in science and society. Previous genetic MPB prediction models were limited by sparse marker coverage, small sample size, and/or data dependency in the different analytical steps. Here, we ... ...

Abstract	Genetic prediction of male pattern baldness (MPB) is important in science and society. Previous genetic MPB prediction models were limited by sparse marker coverage, small sample size, and/or data dependency in the different analytical steps. Here, we present novel models for genetic prediction of MPB based on a large set of markers and large independent subsample sets drawn among 187,435 European subjects. We selected 117 SNP predictors within 85 distinct loci from a list of 270 previously MPB-associated SNPs in 55,573 males of the UK Biobank Study (UKBB). Based on these 117 SNPs with and without age as additional predictor, we trained, by use of different methods, prediction models in a non-overlapping subset of 104,694 UKBB males and tested them in a non-overlapping subset of 26,177 UKBB males. Estimates of prediction accuracy were similar between methods with AUC ranges of 0.725-0.728 for severe, 0.631-0.635 for moderate, 0.598-0.602 for slight, and 0.708-0.711 for no hair loss with age, and slightly lower without, while prediction of any versus no hair loss gave 0.690-0.711 with age and slightly lower without. External validation in an early-onset enriched MPB dataset from the Bonn Study (N = 991) showed improved prediction accuracy without considering age such as AUC of 0.830 for no vs. any hair loss. Because of the large number of markers and the large independent datasets used for the different analytical steps, the newly presented genetic prediction models are the most reliable ones currently available for MPB or any other human appearance trait.
MeSH term(s)	Humans ; Male ; Phenotype ; Alopecia/genetics ; Polymorphism, Single Nucleotide
Language	English
Publishing date	2022-11-07
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	1141470-4
ISSN	1476-5438 ; 1018-4813
ISSN (online)	1476-5438
ISSN	1018-4813
DOI	10.1038/s41431-022-01201-y
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Zs.A 3589: Show issues

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Article ; Online: Mapping of cis-acting expression quantitative trait loci in human scalp hair follicles.

Herrera-Rivero, Marisol / Hochfeld, Lara M / Sivalingam, Sugirthan / Nöthen, Markus M / Heilmann-Heimbach, Stefanie

BMC dermatology

2020 Volume 20, Issue 1, Page(s) 16

Abstract: Background: The association of molecular phenotypes, such as gene transcript levels, with human common genetic variation can help to improve our understanding of interindividual variability of tissue-specific gene regulation and its implications for ... ...

Abstract	Background: The association of molecular phenotypes, such as gene transcript levels, with human common genetic variation can help to improve our understanding of interindividual variability of tissue-specific gene regulation and its implications for disease. Methods: With the aim to capture the spectrum of biological processes affected by regulatory common genetic variants (minor allele frequency ≥ 1%) in healthy hair follicles (HFs) from scalp tissue, we performed a genome-wide mapping of cis-acting expression quantitative trait loci (eQTLs) in plucked HFs, and applied these eQTLs to help further explain genomic findings for hair-related traits. Results: We report 374 high-confidence eQTLs found in occipital scalp tissue, whose associated genes (eGenes) showed enrichments for metabolic, mitotic and immune processes, as well as responses to steroid hormones. We were able to replicate 68 of these associations in a smaller, independent dataset, in either frontal and/or occipital scalp tissue. Furthermore, we found three genomic regions overlapping reported genetic loci for hair shape and hair color. We found evidence to confirm the contributions of PADI3 to human variation in hair traits and suggest a novel potential candidate gene within known loci for androgenetic alopecia. Conclusions: Our study shows that an array of basic cellular functions relevant for hair growth are genetically regulated within the HF, and can be applied to aid the interpretation of interindividual variability on hair traits, as well as genetic findings for common hair disorders.
MeSH term(s)	Adult ; Chromosome Mapping ; Gene Expression Profiling ; Gene Expression Regulation ; Genome-Wide Association Study ; Hair Follicle/growth & development ; Healthy Volunteers ; Humans ; Male ; Polymorphism, Single Nucleotide ; Quantitative Trait Loci ; Regulatory Sequences, Nucleic Acid ; Scalp
Language	English
Publishing date	2020-11-10
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2059863-4
ISSN	1471-5945 ; 1471-5945
ISSN (online)	1471-5945
ISSN	1471-5945
DOI	10.1186/s12895-020-00113-y
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Article ; Online: Hormonal regulation in male androgenetic alopecia-Sex hormones and beyond: Evidence from recent genetic studies.

Heilmann-Heimbach, Stefanie / Hochfeld, Lara M / Henne, Sabrina K / Nöthen, Markus M

Experimental dermatology

2020 Volume 29, Issue 9, Page(s) 814–827

Abstract: Male-pattern hair loss, also termed androgenetic alopecia (AGA), is a highly prevalent age-related condition that is characterized by a distinct pattern of hair loss from the frontotemporal and vertex regions of the scalp. The phenotype is highly ... ...

Abstract	Male-pattern hair loss, also termed androgenetic alopecia (AGA), is a highly prevalent age-related condition that is characterized by a distinct pattern of hair loss from the frontotemporal and vertex regions of the scalp. The phenotype is highly heritable and hormone dependent, with androgens being the recognized critical hormonal factor. Numerous molecular genetic studies have focused on genetic variation in and around the gene that encodes the androgen receptor. More recently, however, the availability of high-throughput molecular genetic methods, novel methods of data analysis and sufficiently large sample sizes have rendered possible the systematic investigation of the contribution of other components of the androgen receptor pathway or hormonal pathways beyond the androgen receptor signalling pathways. Over the past decade, genome-wide association studies of increasingly large cohorts have enabled the genome-wide identification of genetic risk factors for AGA, and yielded unprecedented insights into the underlying pathobiology. The present review discusses some of the most intriguing genetic findings on the relevance of (sex)hormonal signalling in AGA.
MeSH term(s)	Alopecia/genetics ; Alopecia/metabolism ; Hormones/metabolism ; Humans ; Male
Chemical Substances	Hormones
Language	English
Publishing date	2020-07-03
Publishing country	Denmark
Document type	Journal Article ; Review
ZDB-ID	1130936-2
ISSN	1600-0625 ; 0906-6705
ISSN (online)	1600-0625
ISSN	0906-6705
DOI	10.1111/exd.14130
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Article ; Online: Analysis of 72,469 UK Biobank exomes links rare variants to male-pattern hair loss.

Henne, Sabrina Katrin / Aldisi, Rana / Sivalingam, Sugirthan / Hochfeld, Lara Maleen / Borisov, Oleg / Krawitz, Peter Michael / Maj, Carlo / Nöthen, Markus Maria / Heilmann-Heimbach, Stefanie

Nature communications

2023 Volume 14, Issue 1, Page(s) 5492

Abstract: Male-pattern hair loss (MPHL) is common and highly heritable. While genome-wide association studies (GWAS) have generated insights into the contribution of common variants to MPHL etiology, the relevance of rare variants remains unclear. To determine the ...

Abstract	Male-pattern hair loss (MPHL) is common and highly heritable. While genome-wide association studies (GWAS) have generated insights into the contribution of common variants to MPHL etiology, the relevance of rare variants remains unclear. To determine the contribution of rare variants to MPHL etiology, we perform gene-based and single-variant analyses in exome-sequencing data from 72,469 male UK Biobank participants. While our population-level risk prediction suggests that rare variants make only a minor contribution to general MPHL risk, our rare variant collapsing tests identified a total of five significant gene associations. These findings provide additional evidence for previously implicated genes (EDA2R, WNT10A) and highlight novel risk genes at and beyond GWAS loci (HEPH, CEPT1, EIF3F). Furthermore, MPHL-associated genes are enriched for genes considered causal for monogenic trichoses. Together, our findings broaden the MPHL-associated allelic spectrum and provide insights into MPHL pathobiology and a shared basis with monogenic hair loss disorders.
MeSH term(s)	Humans ; Male ; Biological Specimen Banks ; Exome/genetics ; Genome-Wide Association Study ; Alopecia/genetics ; United Kingdom
Language	English
Publishing date	2023-09-22
Publishing country	England
Document type	Journal Article
ZDB-ID	2553671-0
ISSN	2041-1723 ; 2041-1723
ISSN (online)	2041-1723
ISSN	2041-1723
DOI	10.1038/s41467-023-41186-w
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Article ; Online: Abelson Helper Integration Site 1 haplotypes and peripheral blood expression associates with lithium response and immunomodulation in bipolar patients.

Sakrajda, Kosma / Bilska, Karolina / Czerski, Piotr M / Narożna, Beata / Dmitrzak-Węglarz, Monika / Heilmann-Heimbach, Stefanie / Brockschmidt, Felix F / Herms, Stefan / Nöthen, Markus M / Cichon, Sven / Więckowska, Barbara / Rybakowski, Janusz K / Pawlak, Joanna / Szczepankiewicz, Aleksandra

Psychopharmacology

2023 Volume 241, Issue 4, Page(s) 727–738

Abstract: Rationale: In bipolar disorder (BD), immunological factors play a role in the pathogenesis and treatment of the illness. Studies showed the potential link between Abelson Helper Integration Site 1 (AHI1) protein, behavioural changes and innate immunity ... ...

Abstract	Rationale: In bipolar disorder (BD), immunological factors play a role in the pathogenesis and treatment of the illness. Studies showed the potential link between Abelson Helper Integration Site 1 (AHI1) protein, behavioural changes and innate immunity regulation. An immunomodulatory effect was suggested for lithium, a mood stabilizer used in BD treatment. Objectives: We hypothesized that AHI1 may be an important mediator of lithium treatment response. Our study aimed to investigate whether the AHI1 haplotypes and expression associates with lithium treatment response in BD patients. We also examined whether AHI1 expression and lithium treatment correlate with innate inflammatory response genes. Results: We genotyped seven AHI1 single nucleotide polymorphisms in 97 euthymic BD patients and found that TG haplotype (rs7739635, rs9494332) was significantly associated with lithium response. We also showed significantly increased AHI1 expression in the blood of lithium responders compared to non-responders and BD patients compared to healthy controls (HC). We analyzed the expression of genes involved in the innate immune response and inflammatory response regulation (TLR4, CASP4, CASP5, NLRP3, IL1A, IL1B, IL6, IL10, IL18) in 21 lithium-treated BD patients, 20 BD patients treated with other mood stabilizer and 19 HC. We found significantly altered expression between BD patients and HC, but not between BD patients treated with different mood stabilizers. Conclusions: Our study suggests the involvement of AHI1 in the lithium mode of action. Moreover, mood-stabilizing treatment associated with the innate immunity-related gene expression in BD patients and only the lithium-treated BD patients showed significantly elevated expression of anti-inflammatory IL10, suggesting lithium's immunomodulatory potential.
MeSH term(s)	Humans ; Lithium/pharmacology ; Lithium/therapeutic use ; Bipolar Disorder/drug therapy ; Bipolar Disorder/genetics ; Haplotypes ; Interleukin-10 ; Antimanic Agents/therapeutic use ; Lithium Compounds/pharmacology ; Lithium Compounds/therapeutic use
Chemical Substances	Lithium (9FN79X2M3F) ; Interleukin-10 (130068-27-8) ; Antimanic Agents ; Lithium Compounds
Language	English
Publishing date	2023-12-01
Publishing country	Germany
Document type	Journal Article
ZDB-ID	130601-7
ISSN	1432-2072 ; 0033-3158
ISSN (online)	1432-2072
ISSN	0033-3158
DOI	10.1007/s00213-023-06505-5
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Article ; Conference proceedings: Rare but not forgotten – deep molecular and histological characterization of the liver yolk sac tumor and corresponding primary-derived cell line

Castven, Darko / Becker, Diana / Castven, Jovana / Zimpel, Carolin / Heilmann-Heimbach, Stefanie / Roth, Wilfried / Hartmann, Nils / Straub, Beate K. / Lang, Hauke / Galle, Peter R. / Marquardt, Jens Uwe

Zeitschrift für Gastroenterologie

2024 Volume 62, Issue 01

Event/congress	40. Jahrestagung der Deutschen Arbeitsgemeinschaft zum Studium der Leber, Haus der Technik e.V., Essen, 2024-01-26
Language	German
Publishing date	2024-01-01
Publisher	Georg Thieme Verlag
Publishing place	Stuttgart ; New York
Document type	Article ; Conference proceedings
ZDB-ID	201387-3
ISSN	1439-7803 ; 0044-2771 ; 0172-8504
ISSN (online)	1439-7803
ISSN	0044-2771 ; 0172-8504
DOI	10.1055/s-0043-1777588
Database	Thieme publisher's database

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Article ; Online: Evidence for a functional interaction of WNT10A and EBF1 in male-pattern baldness.

Hochfeld, Lara M / Bertolini, Marta / Broadley, David / Botchkareva, Natalia V / Betz, Regina C / Schoch, Susanne / Nöthen, Markus M / Heilmann-Heimbach, Stefanie

PloS one

2021 Volume 16, Issue 9, Page(s) e0256846

Abstract: More than 300 genetic risk loci have been identified for male pattern baldness (MPB) but little is known about the exact molecular mechanisms through which the associated variants exert their effects on MPB pathophysiology. Here, we aimed at further ... ...

Abstract	More than 300 genetic risk loci have been identified for male pattern baldness (MPB) but little is known about the exact molecular mechanisms through which the associated variants exert their effects on MPB pathophysiology. Here, we aimed at further elucidating the regulatory architecture of the MPB risk locus on chromosome (chr.) 2q35, where we have previously reported a regulatory effect of the MPB lead variant on the expression of WNT10A. A HaploReg database research for regulatory annotations revealed that the association signal at 2q35 maps to a binding site for the transcription factor EBF1, whose gene is located at a second MPB risk locus on chr. 5q33.3. To investigate a potential interaction between EBF1 and WNT10A during MPB development, we performed in vitro luciferase reporter assays as well as expression analyses and immunofluorescence co-stainings in microdissected human hair follicles. Our experiments confirm that EBF1 activates the WNT10A promoter and that the WNT10A/EBF1 interaction is impacted by the allelic expression of the MPB risk allele at 2q35. Expression analyses across different hair cycle phases and immunhistochemical (co)stainings against WNT10A and EBF1 suggest a predominant relevance of EBF1/WNT10A interaction for hair shaft formation during anagen. Based on these findings we suggest a functional mechanism at the 2q35 risk locus for MPB, where an MPB-risk allele associated reduction in WNT10A promoter activation via EBF1 results in a decrease in WNT10A expression that eventually results in anagen shortening, that is frequently observed in MPB affected hair follicles. To our knowledge, this study is the first follow-up study on MPB that proves functional interaction between two MPB risk loci and sheds light on the underlying pathophysiological mechanism at these loci.
MeSH term(s)	Alopecia/genetics ; Follow-Up Studies ; Gene Expression Regulation ; Humans ; Male ; Promoter Regions, Genetic ; Trans-Activators/genetics ; Wnt Proteins/genetics
Chemical Substances	EBF1 protein, human ; Trans-Activators ; WNT10A protein, human ; Wnt Proteins
Language	English
Publishing date	2021-09-10
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ISSN	1932-6203
ISSN (online)	1932-6203
DOI	10.1371/journal.pone.0256846
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Article ; Online: Genetic propensity for cerebral amyloidosis and risk of mild cognitive impairment and Alzheimer's disease within a cognitive reserve framework.

Mourtzi, Niki / Charisis, Sokratis / Tsapanou, Angeliki / Ntanasi, Eva / Hatzimanolis, Alexandros / Ramirez, Alfredo / Heilmann-Heimbach, Stefanie / Grenier-Boley, Benjamin / Lambert, Jean-Charles / Yannakoulia, Mary / Kosmidis, Mary / Dardiotis, Efthimios / Hadjigeorgiou, Georgiios / Sakka, Paraskevi / Georgakis, Marios / Yaakov, Stern / Scarmeas, Nikolaos

Alzheimer's & dementia : the journal of the Alzheimer's Association

2023 Volume 19, Issue 9, Page(s) 3794–3805

Abstract: Introduction: We constructed a polygenic risk score (PRS) for β-amyloid (PRSAβ42) to proxy AD pathology and investigated its association with incident Alzheimer's disease (AD)/amnestic mild cognitive impairment (aMCI) and the influence of cognitive ... ...

Abstract	Introduction: We constructed a polygenic risk score (PRS) for β-amyloid (PRSAβ42) to proxy AD pathology and investigated its association with incident Alzheimer's disease (AD)/amnestic mild cognitive impairment (aMCI) and the influence of cognitive reserve (CR), proxied by educational years, on the relationship between PRSAβ42 and AD/aMCI risk. Methods: A total of 618 cognitive-normal participants were followed-up for 2.92 years. The association of PRSAβ42 and CR with AD/aMCI incidence was examined with COX models. Then we examined the additive interaction between PRSAβ42 and CR and the CR effect across participants with different PRSAβ42 levels. Results: Higher PRSAβ42 and CR were associated with a 33.9% higher risk and 8.3% less risk for AD/aMCI, respectively. An additive interaction between PRSAβ42 and CR was observed. High CR was associated with 62.6% less risk of AD/aMCI incidence only in the high-PRSAβ42 group. Discussion: A super-additive effect of PRSAβ42 and CR on AD/aMCI risk was observed. CR influence was evident in participants with high PRSAβ42.
MeSH term(s)	Humans ; Alzheimer Disease/complications ; Cognitive Reserve ; Neuropsychological Tests ; Cognitive Dysfunction/genetics ; Cognitive Dysfunction/complications ; Amyloidosis
Language	English
Publishing date	2023-03-09
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2211627-8
ISSN	1552-5279 ; 1552-5260
ISSN (online)	1552-5279
ISSN	1552-5260
DOI	10.1002/alz.12980
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Article ; Online: A GWAS in Idiopathic/Unexplained Infertile Men Detects a Genomic Region Determining Follicle-Stimulating Hormone Levels.

Schubert, Maria / Pérez Lanuza, Lina / Wöste, Marius / Dugas, Martin / Carmona, F David / Palomino-Morales, Rogelio J / Rassam, Yousif / Heilmann-Heimbach, Stefanie / Tüttelmann, Frank / Kliesch, Sabine / Gromoll, Jörg

The Journal of clinical endocrinology and metabolism

2022 Volume 107, Issue 8, Page(s) 2350–2361

Abstract: Context: Approximately 70% of infertile men are diagnosed with idiopathic (abnormal semen parameters) or unexplained (normozoospermia) infertility, with the common feature of lacking etiologic factors. Follicle-stimulating hormone (FSH) is essential for ...

Abstract	Context: Approximately 70% of infertile men are diagnosed with idiopathic (abnormal semen parameters) or unexplained (normozoospermia) infertility, with the common feature of lacking etiologic factors. Follicle-stimulating hormone (FSH) is essential for initiation and maintenance of spermatogenesis. Certain single-nucleotide variations (SNVs; formerly single-nucleotide polymorphisms [SNPs]) (ie, FSHB c.-211G > T, FSHR c.2039A > G) are associated with FSH, testicular volume, and spermatogenesis. It is unknown to what extent other variants are associated with FSH levels and therewith resemble causative factors for infertility. Objective: We aimed to identify further genetic determinants modulating FSH levels in a cohort of men presenting with idiopathic or unexplained infertility. Methods: We retrospectively (2010-2018) selected 1900 men with idiopathic/unexplained infertility. In the discovery study (n = 760), a genome-wide association study (GWAS) was performed (Infinium PsychArrays) in association with FSH values (Illumina GenomeStudio, v2.0). Minor allele frequencies (MAFs) were analyzed for the discovery and an independent normozoospermic cohort. In the validation study (n = 1140), TaqMan SNV polymerase chain reaction was conducted for rs11031005 and rs10835638 in association with andrological parameters. Results: Imputation revealed 9 SNVs in high linkage disequilibrium, with genome-wide significance (P < 4.28e-07) at the FSHB locus 11p.14.1 being associated with FSH. The 9 SNVs accounted for up to a 4.65% variance in FSH level. In the oligozoospermic subgroup, this was increased up to 6.95% and the MAF was enhanced compared to an independent cohort of normozoospermic men. By validation, a significant association for rs11031005/rs10835638 with FSH (P = 4.71e-06/5.55e-07) and FSH/luteinizing hormone ratio (P = 2.08e-12/6.4e-12) was evident. Conclusions: This GWAS delineates the polymorphic FSHB genomic region as the main determinant of FSH levels in men with unexplained or idiopathic infertility. Given the essential role of FSH, molecular detection of one of the identified SNVs that causes lowered FSH and therewith decreases spermatogenesis could resolve the idiopathic/unexplained origin by this etiologic factor.
MeSH term(s)	Humans ; Male ; Follicle Stimulating Hormone/blood ; Genome-Wide Association Study ; Genomics ; Infertility, Male/genetics ; Polymorphism, Single Nucleotide ; Retrospective Studies
Chemical Substances	Follicle Stimulating Hormone (9002-68-0)
Language	English
Publishing date	2022-03-01
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	3029-6
ISSN	1945-7197 ; 0021-972X
ISSN (online)	1945-7197
ISSN	0021-972X
DOI	10.1210/clinem/dgac165
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