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From in vivo to in vitro: exploring the key molecular and cellular aspects of human female gametogenesis

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Abstract

Human oogenesis is a highly complex and not yet fully understood process due to ethical and technological barriers that limit studies in the field. In this context, replicating female gametogenesis in vitro would not only provide a solution for some infertility problems, but also be an excellent study model to better understand the biological mechanisms that determine the formation of the female germline. In this review, we explore the main cellular and molecular aspects involved in human oogenesis and folliculogenesis in vivo, from the specification of primordial germ cells (PGCs) to the formation of the mature oocyte. We also sought to describe the important bidirectional relationship between the germ cell and the follicular somatic cells. Finally, we address the main advances and different methodologies used in the search for obtaining cells of the female germline in vitro.

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Data availability

The data that support the findings of this study are available on request from the corresponding author.

Abbreviations

5hmc:

5-Hydroxymethylcytosine

AFF1:

ALF Transcription Elongation Factor 1

ALKs:

Activin-like kinases

AMH:

Anti-mullerian hormone

ART:

Assisted reproduction techniques

BLIMP1:

Lymphocyte-induced maturation protein-1

BMP15:

Bone morphogenetic protein 15

BMP6:

Bone morphogenetic protein 6

BMPs:

Bone morphogenetic proteins

BOULE:

Boule Homolog, RNA Binding Protein

cAMP:

Cyclic-adenosine-monophosphate

CCs:

Cumulus cells

CDK1:

Cyclin Dependent Kinase 1

cGMP:

Cyclic guanosine monophosphate

CNP:

C-type natriuretic peptide

Co-Smads:

Commun Smads

CSDE1:

Cold Shock Domain Containing E1

CYP26B1:

Cytochrome P450 26B1

DAX1:

Dosage-Sensitive Sex-Reversal-AHC Critical Region on the X Chromosome

DAZL:

Deleted In Azoospermia Like

DDX4:

XXX

DNA:

Deoxyribonucleic acid

DND:

MicroRNA-Mediated Repression Inhibitor 1

DNMT3A:

DNA Methyltransferase 3 Alpha

DNMT3B:

DNA Methyltransferase 3 Beta

DPPA3:

DEAD-Box Helicase 4

DPPA3:

Developmental Pluripotency Associated 3

EB:

Embryoid body

EGF:

Epidermal growth factor

EOMES:

Eomesodermin

ESCs / hESCs:

Embryonic stem cells / human embryonic stem cells

ETV5:

ETS Variant Transcription Factor 5

FGF2:

Fibroblast Growth Factor 2

FGF8:

Fibroblast Growth Factor 8

FGF9:

Fibroblast Growth Factor 9

FGFCs:

Female germline stem cells

FGG:

Fibrinogen Gamma Chain

FIGLA:

Folliculogenesis-Specific Basic Helix-Loop-Helix Protein.

FLS:

Follicle-like structures

FOXD1:

Forkhead Box D1

FOXL2:

Forkhead box L2

FOXO6:

Forkhead Box O6

FSH:

Follicle-stimulating hormone

GATA3:

GATA binding protein 3

GATA4:

GATA binding protein 4

GCLCs:

Granulosa cells like-cells

GCs:

Granulosa cells

GDF9:

Growth Differentiation Factor 9

GH:

Growth hormone

GREM1:

Gremlin 1, DAN Family BMP Antagonist

GSK3:

Glycogen Synthase Kinase 3

GTF2I:

General Transcription Factor IIi

GV:

Germinal vesicle

GVBD:

Germinal vesicle breaking down

H1FOO:

H1 Histone Family, Member O, Oocyte-Specific

H3K27me 3:

Histone H3 lysine 27 tri-methylation

H3K9me2:

H3 lysine 9 di-methylation

HAS2:

Hyaluronan Synthase 2

HBP1:

HMG-Box Transcription Factor 1

hCG:

Human chorionic gonadotropin

HES6:

Hes Family BHLH Transcription Factor 6

HIF1A:

Hypoxia Inducible Factor 1 Subunit Alpha

HMBG3:

High Mobility Group Box 3

hOLCs:

Human oocyte-like cells

HOXA5:

Homeobox A5

HOXB6:

Homeobox B6

ID3:

Inhibitor of DNA binding 3

IGFBP5:

Insulin-like growth factor binding protein 5

iMeLCs:

Incipient mesoderm-like cells

iPSCs / hiPSCs:

Induced pluripotent stem cells / human induced pluripotent stem cells

ITGB3:

Integrin subunit beta 3

JARID2:

Jumonji and AT-rich interaction domain containing 2

JNK:

C-Jun N-terminal kinase

KIT:

KIT Proto-Oncogene, Receptor Tyrosine Kinase

KITL:

KIT ligand

KLF2:

KLF transcription factor 2

LH:

Luteinizing hormone

LIF:

Leukemia Inhibitory Factor

MAEL:

Maelstrom spermatogenic transposon silencer

MAPK:

Mitogen-activated protein kinase

mGCs:

Mural granulosa cells

MVH:

Mouse vasa homolog

miRNAs:

Micro RNAs

MPF:

Maturation promoting factor

mRNAs:

Messenger RNAs

NANOS:

Nanos C2HC-Type Zinc Finger

NANOS3:

Nanos C2HC-Type Zinc Finger 3

NFKB2:

Nuclear factor kappa b subunit 2

NOBOX:

Homeobox protein NOBOX

NPPC:

Natriuretic peptide C

NPR2:

Natriuretic peptide receptor 2

NR3C2:

Nuclear receptor subfamily 3 group C member 2

NR5A1:

Nuclear receptor subfamily 5 group A member 1

OTX2:

Orthodenticle Homeobox 2

PBX1:

PBX Homeobox 1

PGCLCs/ hPGCLCs:

Primordial germ cells like-cells / human primordial germ cells like-cells

PGCs:

Primordial germ cells

PI3K:

Phosphatidylinositol-4,5-bisphosphate 3-kinase catalytic subunit alpha

PINX1:

PIN2 (TERF1) interacting telomerase inhibitor 1

PIWIL2:

Piwi-like RNA-mediated gene silencing 2

PKA:

Protein kinase A

PNCK:

Pregnancy up-regulated nonubiquitous CaM kinase

PROK2:

Prokineticin 2

PTEN:

Phosphatase and tensin homolog

PTGS2:

Prostaglandin-endoperoxide synthase 2

PTX3:

Pentraxin 3

RAD51AP2:

RAD51 associated protein 2

RARB:

Retinoic acid receptor beta

REC8:

REC8 Meiotic recombination protein

RNA:

Ribonucleic acid

RUNX1:

Runt-related transcription factor 1

RUNX2:

Runt-related transcription factor 2

RYR2:

Ryanodine receptor 2

SCF:

Stem cell factor

SCP3:

Synaptonemal Complex Protein 3

Smads-R:

Response Smads

SMARCE1:

SWI/SNF related, matrix associated, actin-dependent regulator of Chromatin, Subfamily E, member 1

SOHLH2:

Spermatogenesis and oogenesis specific basic helix-loop-helix 2

SOX13:

SRY-box transcription factor 13

SOX17:

SRY-box transcription factor 17

SOX30:

SRY-box transcription factor 30

SPO11:

SRY-box transcription factor 11

SRY:

Sex-determining region Y

StAR:

Steroidogenic acute regulatory protein

STAT1:

Signal transducer and activator of transcription 1

STELLA:

Stella-related protein

STRA8:

Stimulated by retinoic acid 8

TBX3:

T-Box transcription factor 3

TCs:

Theca cells

TDRD6:

Tudor domain containing 6

TEAD2:

TEA domain transcription factor 2

TERT:

Telomerase reverse transcriptase

TEX12:

Testis expressed 12

TEX14:

Testis expressed 14

TFAP2C:

Transcription Factor AP-2 Gamma

TGFα:

Transforming growth factor alpha

TGFβ:

Transforming growth factor beta

TSPAN8:

Tetraspanin 8

TUB:

TUB Bipartite transcription factor

TZPs:

Transzonal projections

UHRF1:

Ubiquitin like with PHD and ring finger domains 1

UTF1:

Undifferentiated embryonic cell transcription factor 1

WNT3A:

Protein Wnt-3a

WNT4:

Wnt family member 4

WT1:

Wilms Tumor 1

YBX2:

Y-Box Binding Protein 2

ZBTB11:

Zinc finger and btb domain containing 11

ZGLP1:

Zinc finger GATA like protein 1

ZIC1:

Zic Family member 1

ZNF362:

Zinc finger protein 362

ZNF98:

Zinc finger protein 98

ZP2:

Zona pellucida glycoprotein 2

ZP3:

Zona pellucida glycoprotein 3

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Acknowledgements

The authors thank the support from CAPES, FAPEMIG (RED-00135-2- REDE MINEIRA DE INTELIGÊNCIA ARTIFICIAL NA REPRODUÇÃO HUMANA and RED-00079-22- REDE MINEIRA DE NANOMEDICINA TERANÓSTICA) and CNPq (scholarship granted to S.A.C.). We also acknowledge the Center for Image Acquisition and Processing of the Institute of Biological Sciences at UFMG (CAPI, ICB/UFMG) and Clínica Cegonha de Medicina Reprodutiva.

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  1. Laboratory of Cellular Biology, Department of Morphology, Institute of Biological Sciences, Federal University of Minas Gerais, Belo Horizonte, MG, 31270-901, Brazil

    Sarah Abreu Coxir, Guilherme Mattos Jardim Costa, Camilla Fernandes dos Santos & Samyra Maria dos Santos Nassif Lacerda

  2. Clínica Cegonha de Medicina Reprodutiva, Belo Horizonte, MG, 30160-030, Brazil

    Raquel de Lima Leite Soares Alvarenga

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Coxir, S.A., Costa, G.M.J., Santos, C.F.d. et al. From in vivo to in vitro: exploring the key molecular and cellular aspects of human female gametogenesis. Human Cell 36, 1283–1311 (2023). https://doi.org/10.1007/s13577-023-00921-7

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