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Article: Insights into Germline Development and Differentiation in Molluscs and Reptiles: The Use of Molecular Markers in the Study of Non-model Animals.

Milani, Liliana / Maurizii, Maria Gabriella

Results and problems in cell differentiation

2019 Volume 68, Page(s) 321–353

Abstract: When shifting research focus from model to non-model species, many differences in the working approach should be taken into account and usually methodological modifications are required because of the lack of genetics/genomics and developmental ... ...

Abstract	When shifting research focus from model to non-model species, many differences in the working approach should be taken into account and usually methodological modifications are required because of the lack of genetics/genomics and developmental information for the vast majority of organisms. This lack of data accounts for the largely incomplete understanding of how the two components-genes and developmental programs-are intermingled in the process of evolution. A deeper level of knowledge was reached for a few model animals, making it possible to understand some of the processes that guide developmental changes during evolutionary time. However, it is often difficult to transfer the obtained information to other, even closely related, animals. In this chapter, we present and discuss some examples, such as the choice of molecular markers to be used to characterize differentiation and developmental processes. The chosen examples pertain to the study of germline in molluscs, reptiles, and other non-model animals.
MeSH term(s)	Animals ; Biomarkers/analysis ; Biomarkers/metabolism ; Cell Differentiation ; Germ Cells/cytology ; Germ Cells/metabolism ; Mollusca/cytology ; Reptiles/embryology
Chemical Substances	Biomarkers
Language	English
Publishing date	2019-10-09
Publishing country	Germany
Document type	Journal Article ; Review
ISSN	0080-1844
ISSN	0080-1844
DOI	10.1007/978-3-030-23459-1_14
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Article ; Online: Immunohistochemical Analysis of Olfactory Sensory Neuron Populations in the Developing Olfactory Organ of the Guppy, Poecilia reticulata (Cyprinodontiformes, Poecilidae).

Bettini, Simone / Lazzari, Maurizio / Milani, Liliana / Maurizii, Maria Gabriella / Franceschini, Valeria

Microscopy and microanalysis : the official journal of Microscopy Society of America, Microbeam Analysis Society, Microscopical Society of Canada

2023 Volume 29, Issue 5, Page(s) 1764–1773

Abstract: Olfaction is fundamental for sensing environmental chemicals and has obvious adaptive advantages. In fish, the peripheral olfactory organ is composed of lamellae in which the olfactory mucosa contains three main categories of olfactory sensory neurons ( ... ...

Abstract	Olfaction is fundamental for sensing environmental chemicals and has obvious adaptive advantages. In fish, the peripheral olfactory organ is composed of lamellae in which the olfactory mucosa contains three main categories of olfactory sensory neurons (OSNs) as follows: ciliated (cOSNs), microvillous (mOSNs), and crypt cells. We studied the appearance of these different OSNs during development of Poecilia reticulata, given its growing use as animal model system. We performed immunohistochemical detection of molecular markers specific for the different OSNs, carrying out image analyses for marked-cell counting and measuring optical density. The P. reticulata olfactory organ did not show change in size during the first weeks of life. The proliferative activity increased at the onset of secondary sexual characters, remaining high until sexual maturity. Then, it decreased in both sexes, but with a recovery in females, probably in relation to their almost double body growth, compared to males. The density of both cOSNs and mOSNs remained constant throughout development, probably due to conserved functions already active in the fry, independently of the sex. The density of calretinin-positive crypt cells decreased progressively until sexual maturity, whereas the increased density of calretinin-negative crypt cell fraction, prevailing in later developmental stages, indicated their probable involvement in reproductive activities.
MeSH term(s)	Animals ; Female ; Male ; Olfactory Receptor Neurons ; Poecilia ; Calbindin 2 ; Olfactory Mucosa
Chemical Substances	Calbindin 2
Language	English
Publishing date	2023-08-28
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	1385710-1
ISSN	1435-8115 ; 1431-9276
ISSN (online)	1435-8115
ISSN	1431-9276
DOI	10.1093/micmic/ozad099
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Article: Analysis of

Ricci, Serena / Lazzari, Maurizio / Maurizii, Maria Gabriella / Franceschini, Valeria / Milani, Liliana / Cacialli, Pietro

Animals : an open access journal from MDPI

2023 Volume 13, Issue 23

Abstract: Cytoplasmic linker-associated protein-2 (CLASP2) is a member of the CLIP-associating proteins (CLASPs) family involved in the structure and function of microtubules and Golgi apparatus. Several studies performed using different mammalian and non- ... ...

Abstract	Cytoplasmic linker-associated protein-2 (CLASP2) is a member of the CLIP-associating proteins (CLASPs) family involved in the structure and function of microtubules and Golgi apparatus. Several studies performed using different mammalian and non-mammalian model organisms reported that CLASP2 controls microtubule dynamics and the organization of microtubule networks. In
Language	English
Publishing date	2023-11-22
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2606558-7
ISSN	2076-2615
ISSN	2076-2615
DOI	10.3390/ani13233617
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Article ; Online: Vasa expression in spermatogenic cells during the reproductive-cycle phases of Podarcis sicula (Reptilia, Lacertidae).

Milani, Liliana / Maurizii, Maria Gabriella

Journal of experimental zoology. Part B, Molecular and developmental evolution

2015 Volume 324, Issue 5, Page(s) 424–434

Abstract: The vasa gene encodes a DEAD-box ATP-dependent RNA helicase that regulates the translation of multiple mRNAs involved in germ line differentiation. This protein has been deeply studied in many animals, but few data are available to date on reptiles. In ... ...

Abstract	The vasa gene encodes a DEAD-box ATP-dependent RNA helicase that regulates the translation of multiple mRNAs involved in germ line differentiation. This protein has been deeply studied in many animals, but few data are available to date on reptiles. In this work, we sequenced a portion of Podarcis sicula vasa gene (Ps-vasa), developed a specific antibody and verified its specificity. Using anti-Ps-Vasa and confocal microscopy, we studied Vasa expression in male germ cells during the reproductive cycle of P. sicula: during full gonadal activity (spring), during regression of gonadal activity (summer) and during slow autumnal recrudescence. We also analyzed Vasa expression in young testes when the walls of the seminiferous tubules were forming. The aim was to verify if Vasa is involved in the process of male germ cell differentiation in all phases of the reproductive cycle. In adult testes, during full gonadal activity and during recrudescence, Vasa staining was detected from spermatogonia to spermatids. Vasa spots were also observed in the nucleus of germ cells supporting its function in different cellular compartments. No Vasa staining was observed in mature spermatozoa during the spring and mid-late November. The seminiferous epithelium analyzed in the summer appeared reduced with only spermatogonia, all Vasa-immunostained, some in division to replace germ cells. In immature testes, the seminiferous epithelium contained only spermatogonia and spermatocytes. The clear immunostaining in their cytoplasm revealed that Vasa is already expressed in juvenile male gonads, suggesting a role in the differentiation process since P. sicula early developmental stages.
MeSH term(s)	Amino Acid Sequence ; Animals ; DEAD-box RNA Helicases/genetics ; DEAD-box RNA Helicases/metabolism ; Female ; Gene Expression Regulation, Developmental ; Lizards/genetics ; Male ; Molecular Sequence Data ; Oogenesis/genetics ; Ovary/cytology ; Ovary/metabolism ; Reproduction/genetics ; Reproduction/physiology ; Seasons ; Spermatogenesis/genetics ; Testis/cytology ; Testis/metabolism
Chemical Substances	DEAD-box RNA Helicases (EC 3.6.4.13)
Language	English
Publishing date	2015-07
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2103823-5
ISSN	1552-5015 ; 0022-104X ; 1552-5007
ISSN (online)	1552-5015
ISSN	0022-104X ; 1552-5007
DOI	10.1002/jez.b.22628
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Article ; Online: First evidence of Vasa expression in differentiating male germ cells of a reptile.

Milani, Liliana / Maurizii, Maria Gabriella

Molecular reproduction and development

2014 Volume 81, Issue 8, Page(s) 678

MeSH term(s)	Animals ; DEAD-box RNA Helicases/metabolism ; Gene Expression Profiling ; Lizards/genetics ; Lizards/metabolism ; Male ; Microscopy, Confocal ; Spermatogenesis/physiology ; Spermatozoa/metabolism ; Spermatozoa/physiology
Chemical Substances	DEAD-box RNA Helicases (EC 3.6.4.13)
Language	English
Publishing date	2014-08
Publishing country	United States
Document type	Letter
ZDB-ID	20321-x
ISSN	1098-2795 ; 1040-452X
ISSN (online)	1098-2795
ISSN	1040-452X
DOI	10.1002/mrd.22349
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Article ; Online: Early germline differentiation in bivalves: TDRD7 as a candidate investigational unit for Ruditapes philippinarum germ granule assembly.

Filanti, Beatrice / Piccinini, Giovanni / Bettini, Simone / Lazzari, Maurizio / Franceschini, Valeria / Maurizii, Maria Gabriella / Milani, Liliana

Histochemistry and cell biology

2021 Volume 156, Issue 1, Page(s) 19–34

Abstract: The germline is a key feature of sexual animals and the ways in which it separates from the soma differ widely across Metazoa. However, at least at some point during germline differentiation, some cytoplasmic supramolecular structures (collectively ... ...

Abstract	The germline is a key feature of sexual animals and the ways in which it separates from the soma differ widely across Metazoa. However, at least at some point during germline differentiation, some cytoplasmic supramolecular structures (collectively called germ plasm-related structures) are present and involved in its specification and/or differentiation. The factors involved in the assembly of these granular structures are various and non-ubiquitous among animals, even if some functional patterns and the presence of certain domains appear to be shared among some. For instance, the LOTUS domain is shared by Oskar, the Holometabola germ plasm master regulator, and some Tudor-family proteins assessed as being involved in the proper assembly of germ granules of different animals. Here, we looked for the presence of LOTUS-containing proteins in the transcriptome of Ruditapes philippinarum (Bivalvia). Such species is of particular interest because it displays annual renewal of gonads, sided by the renewal of germline differentiation pathways. Moreover, previous works have identified in its early germ cells cytoplasmic granules containing germline determinants. We selected the orthologue of TDRD7 as a candidate involved in the early steps of germline differentiation through bioinformatic predictions and immunohistological patterning (immunohistochemistry and immunofluorescence). We observed the expression of the protein in putative precursors of germline cells, upstream to the germline marker Vasa. This, added to the fact that orthologues of this protein are involved in the assembly of germ granules in mouse, zebrafish, and fly, makes it a worthy study unit for investigations on the formation of such structures in bivalves.
MeSH term(s)	Animals ; Bivalvia ; Cell Differentiation ; Cytoplasmic Granules/metabolism ; Germ Cells/cytology ; Germ Cells/metabolism ; Ribonucleoproteins/analysis ; Ribonucleoproteins/metabolism
Chemical Substances	Ribonucleoproteins
Language	English
Publishing date	2021-03-26
Publishing country	Germany
Document type	Journal Article
ZDB-ID	1222930-1
ISSN	1432-119X ; 0301-5564 ; 0948-6143
ISSN (online)	1432-119X
ISSN	0301-5564 ; 0948-6143
DOI	10.1007/s00418-021-01983-0
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Article ; Online: Microtubule organization and nucleation in the differentiating ovarian follicle of the lizard Podarcis sicula.

Maurizii, Maria Gabriella / Taddei, Carlo

Journal of morphology

2012 Volume 273, Issue 10, Page(s) 1089–1095

Abstract: We analyzed the organization of the microtubular cytoskeleton and the distribution of centrosomes at the different stages of differentiation of the ovarian follicle of the lizard Podarcis sicula by examining immunolabeled α- and γ-tubulins using confocal ...

Abstract	We analyzed the organization of the microtubular cytoskeleton and the distribution of centrosomes at the different stages of differentiation of the ovarian follicle of the lizard Podarcis sicula by examining immunolabeled α- and γ-tubulins using confocal microscopy. We observed that in the follicular epithelium the differentiation of the nurse pyriform cells is accompanied by a reorganization of the microtubules in the oocyte cortex, changing from a reticular to a radial pattern. Furthermore, these cortical microtubules extend in the cytoplasm of the connected follicle cells through intercellular bridges. Radially oriented microtubules were still more marked in the oocyte cortex during the final stages of oogenesis, when the yolk proteins were incorporated by endocytosis. The nucleation centres of the microtubules (centrosomes) were clearly detectable as γ-tubulin immunolabeled spots in the somatic stromal cells of the germinal bed. A diffuse cytoplasmic immunolabeling together with multiple labeled foci, resembling the desegregation of the centrosomes in early oogenesis of vertebrates and invertebrates, was revealed in the prediplotenic germ cells. In the cytoplasm of growing oocytes, a diffuse labeling of the γ-tubulin antibody was always detectable. In the growing ovarian follicles, immunolabeled spots were detected in the mono-layered follicle cells which surrounded the early oocytes. In follicles with a polymorphic follicular epithelium, only the small follicle cells showed labeled spots. A weak and diffuse labeling was observed in the pyriform cells while in the enlarging intermediate cells the centrosomes degenerated like in the early oocytes. Our observations confirm that in P. sicula most of the oocyte growth is supported by the structural and functional integration of the developing oocyte with the pyriform nurse cells and suggest that their fusion with the oocyte results in an acquirement by these somatic cells of characteristics typical of the germ cells.
MeSH term(s)	Animals ; Cell Differentiation ; Centrosome ; Cytoplasm/metabolism ; Cytoskeleton/metabolism ; Female ; Lizards/anatomy & histology ; Microtubules ; Oocytes/cytology ; Oocytes/growth & development ; Oocytes/metabolism ; Oocytes/ultrastructure ; Oogenesis ; Ovarian Follicle/ultrastructure ; Tubulin/metabolism
Chemical Substances	Tubulin
Language	English
Publishing date	2012-10
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	3084-3
ISSN	1097-4687 ; 0022-2887 ; 0362-2525
ISSN (online)	1097-4687
ISSN	0022-2887 ; 0362-2525
DOI	10.1002/jmor.20046
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Article ; Online: PL10 DEAD-Box Protein is Expressed during Germ Cell Differentiation in the Reptile Podarcis sicula (Family Lacertidae).

Milani, Liliana / Pecci, Andrea / Cifaldi, Carmine / Maurizii, Maria Gabriella

Journal of experimental zoology. Part B, Molecular and developmental evolution

2017 Volume 328, Issue 5, Page(s) 433–448

Abstract: Among genes involved in the regulation of germ cell differentiation, those of DDX4/Vasa and the Ded1/DDX3 subfamilies encode for DEAD-box ATP-dependent RNA helicases, proteins involved in many mechanisms related to RNA processing. For the first time in ... ...

Abstract	Among genes involved in the regulation of germ cell differentiation, those of DDX4/Vasa and the Ded1/DDX3 subfamilies encode for DEAD-box ATP-dependent RNA helicases, proteins involved in many mechanisms related to RNA processing. For the first time in reptiles, using specific antibodies at confocal microscopy, we analysed the localization pattern of a Ded1/DDX3 subfamily member in testis and ovary of Podarcis sicula (Ps-PL10) during the reproductive cycle. In testis, Ps-PL10 is expressed in the cytoplasm of spermatocytes and it is not detected in spermatogonia. Differently from Ps-VASA, in round spermatids, Ps-PL10 is not segregated in the chromatoid body but it accumulates in the cytoplasm of residual bodies, and mature spermatozoa are unstained. These observations suggest that in males, Ps-PL10 (1) is involved in spermatogenesis and (2) is then eliminated with residual bodies. In the ovary, Ps-PL10 is present with granules in the cytoplasm of early meiotic cells of the germinal bed (GB), while it is not present in oogonia and somatic cells of the GB stroma. In follicular cells of ovarian follicles, Ps-PL10 expression starts after their fusion with the oocyte. Numerous Ps-PL10 spots are visible in pyriform (nurse-like) cells concomitantly with the protein accumulation in the cytoplasm of differentiating oocyte. In pyriform cells, Ps-PL10 spots are present in the cytoplasm and nuclei, as observed for Ps-VASA, and in the nucleoli, suggesting for Ps-PL10 a role in rRNA processing and in the transport of molecules from the nucleus to cytoplasm and from nurse cells to the oocyte.
MeSH term(s)	Amino Acid Sequence ; Animals ; Antibodies ; Antibody Specificity ; Cell Differentiation/physiology ; DEAD-box RNA Helicases/genetics ; DEAD-box RNA Helicases/metabolism ; Female ; Gene Expression Regulation, Enzymologic/physiology ; Germ Cells/physiology ; Lizards/genetics ; Lizards/metabolism ; Male ; Microscopy, Confocal ; Phylogeny
Chemical Substances	Antibodies ; DEAD-box RNA Helicases (EC 3.6.4.13)
Language	English
Publishing date	2017-06-27
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2103823-5
ISSN	1552-5015 ; 0022-104X ; 1552-5007
ISSN (online)	1552-5015
ISSN	0022-104X ; 1552-5007
DOI	10.1002/jez.b.22744
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Article ; Online: Differential nickel-induced responses of olfactory sensory neuron populations in zebrafish.

Lazzari, Maurizio / Bettini, Simone / Milani, Liliana / Maurizii, Maria Gabriella / Franceschini, Valeria

Aquatic toxicology (Amsterdam, Netherlands)

2018 Volume 206, Page(s) 14–23

Abstract: The olfactory epithelium of fish includes three main types of olfactory sensory neurons (OSNs). Whereas ciliated (cOSNs) and microvillous olfactory sensory neurons (mOSNs) are common to all vertebrates, a third, smaller group, the crypt cells, is ... ...

Abstract	The olfactory epithelium of fish includes three main types of olfactory sensory neurons (OSNs). Whereas ciliated (cOSNs) and microvillous olfactory sensory neurons (mOSNs) are common to all vertebrates, a third, smaller group, the crypt cells, is exclusive for fish. Dissolved pollutants reach OSNs, thus resulting in impairment of the olfactory function with possible neurobehavioral damages, and nickel represents a diffuse olfactory toxicant. We studied the effects of three sublethal Ni
MeSH term(s)	Animals ; GTP-Binding Protein alpha Subunits/metabolism ; Nickel/toxicity ; Olfactory Mucosa/drug effects ; Olfactory Receptor Neurons/drug effects ; Water Pollutants, Chemical/toxicity ; Zebrafish/physiology
Chemical Substances	GTP-Binding Protein alpha Subunits ; Water Pollutants, Chemical ; olfactory G protein subunit alpha olf ; Nickel (7OV03QG267)
Language	English
Publishing date	2018-10-23
Publishing country	Netherlands
Document type	Journal Article
ZDB-ID	782699-0
ISSN	1879-1514 ; 0166-445X
ISSN (online)	1879-1514
ISSN	0166-445X
DOI	10.1016/j.aquatox.2018.10.011
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Article ; Online: Crypt cell markers in the olfactory organ of Poecilia reticulata: analysis and comparison with the fish model Danio rerio.

Bettini, Simone / Milani, Liliana / Lazzari, Maurizio / Maurizii, Maria Gabriella / Franceschini, Valeria

Brain structure & function

2017 Volume 222, Issue 7, Page(s) 3063–3074

Abstract: Olfactory crypt neurons have been observed in several bony fishes and chondrichtyans. Although their morphology is uniform in all fish, very few is known about their antigenic properties, usually studied in zebrafish, but quite overlooked in other ... ...

Abstract	Olfactory crypt neurons have been observed in several bony fishes and chondrichtyans. Although their morphology is uniform in all fish, very few is known about their antigenic properties, usually studied in zebrafish, but quite overlooked in other species. We tested in Poecilia reticulata (guppy) the two antibodies recognized to mark zebrafish crypt cells: while anti-S100 showed an immunohistochemical pattern comparable to what reported in zebrafish, anti-TrkA gave no signal. Western blot analysis revealed that S100-antiserum bound an antigen of expected weight, probably belonging to the S100 family. On the contrary, anti-TrkA detected more bands, but the protein/s might be too much diffused and/or diluted in the tissue to be detected with immunohistochemistry. Because of the high level of conservation in the Trk family proteins of the kinase domain, on which anti-TrkA was produced, we also tested anti-TrkB to exclude cross reactivity. Immunohistochemistry and Western blot confirmed that anti-TrkB displayed high specificity to its target and a different staining pattern compared to anti-TrkA, but, as anti-TrkA, it did not label crypt neurons. Finally, we documented that calretinin, a known marker of zebrafish ciliated and microvillous olfactory cells, in the guppy is expressed also by a subpopulation of S100-positive crypt neurons. These results reveal differences in antigen expression between zebrafish and guppy crypt cells. Together with the already known species-specific projections to the olfactory bulb and a heterogeneous panel of odorants, our findings support the possibility that crypt cells are functionally less uniform as supposed.
MeSH term(s)	Animals ; Brain/cytology ; Calbindin 2/metabolism ; Female ; Microscopy, Electron, Transmission ; Neurons/metabolism ; Neurons/ultrastructure ; Olfactory Bulb/cytology ; Olfactory Pathways/metabolism ; Olfactory Pathways/ultrastructure ; Poecilia/anatomy & histology ; Receptor, trkB/metabolism ; S100 Proteins/metabolism ; Species Specificity ; Zebrafish/anatomy & histology
Chemical Substances	Calbindin 2 ; S100 Proteins ; Receptor, trkB (EC 2.7.10.1)
Language	English
Publishing date	2017-03-09
Publishing country	Germany
Document type	Journal Article
ZDB-ID	2273162-3
ISSN	1863-2661 ; 1863-2653
ISSN (online)	1863-2661
ISSN	1863-2653
DOI	10.1007/s00429-017-1386-2
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