Abstract
Primordial Germ Cells (PGC) are the progenitors of the germ-line and differentiate into spermatozoa or oocytes. They are responsible for the transmission of genetic and epigenetic information from one generation to the other. Since the nineteenth century, PGCs have been investigated using different techniques. Regardless of their mode of specification, inheritance or induction, PGCs arise early in development and migrate by a combination of passive and active movements towards the gonadic ridges. The migration of PGCs is very similar to the path taken by metastasis and germ cells are very often proposed as a model for the study of cell migration. Their pathway of migration is regulated by different signals that interact with Hsp90, an ATP-dependent chaperone associated with numerous tumors and used to grade the malignancy. Furthermore, some of the signals regulating PGCs have been proved to have a role in different cancers. This underlines the idea that PGCs could be an interesting tool to study long-distance cell migration and perhaps cancer.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Abbreviations
- actr2:
-
Actin related protein 2 homolog
- alk2:
-
Activin receptor-like kinase-2
- Bmp:
-
Bone morphogenetic proteins
- Bmpr:
-
Bone morphogenetic protein receptor
- EMT:
-
Epithelial-mesenchymal transition
- GR:
-
Gonadal ridge
- Hsp:
-
Heat shock protein
- MOTC:
-
Microtubule organizer center
- PGC:
-
Primordial germ cells
- ROCK/RhoA:
-
Rho-associated protein kinase
- TGFβ:
-
Transforming growth factor β
References
Ara T, Nakamura Y, Egawa T, Sugiyama T, Abe K, Kishimoto T, Matsui Y, Nagasawa T (2003) Impaired colonization of the gonads by primordial gem cells in mice lacking a chemokine, stromal cell-derived factor-1 (SDF-1). Proc Natl Acad Sci 100:5319–5323
Bendel-Stenze MR, Gomperts M, Anderson R, Heasman J, Wylie C (2000) The role of cadherins during primordial germ cell migration and early gonad formation in the mouse. Mech Dev 91:143–152
Buchner J (1999) HSP90 & Co.-a holding for folding. Trends Biochem Sci 24:136–141
Castrillon DH, Quade BJ, Wang TY, Quigley C, Crum CP (2000) The human VASA gene is specifically expressed in the germ cell lineage. Proc Natl Acad Sci U S A 97:9585–9590
Chen WS, Chen CC, Chen LL, Lee CC, Huang TS (2013) Secreted heat shock protein 90α (HSP90α) induces nuclear factor-κB-mediated TCF12 protein expression to down-regulate E-cadherin and to enhance colorectal cancer cell migration and invasion. J Biol Chem 288:9001–9010
Chiquoine DA (1954) The identification, origin, and migration of the primordial germ cells in the mouse embryo. Anat Rec 118:135–146
D’Costa S, Petitte JN (1999) Characterization of stage-specific embryonic antigen-1 (SSEA-1) expression during early development of the turkey embryo. Int J Dev Biol 43:349–356
De Felici M (2013) Origin, migration, and proliferation of human primordial germ cells. In: Coticchio B, De Santis L (eds) Oogenesis. Springer, London, pp 19–37
Deborah LR, Bennett LK (1993) glh-1, a germ-line putative RNA helicase from Caenorhabditis, has four zinc fingers. Proc Natl Acad Sci U S A 90:9300–9304
Doitsidou M, Reichman-Fried M, Stebler J, Koprunner M, Dorries J, Meyer D, Esguerra CV, Leung T, Raz E (2002) Guidance of primordial germ cell migration by the chemokine SDF-1. Cell 111:647–659
Dudley BM, Runyan C, Takeuchi Y, Schaible K, Molyneaux K (2007) BMP signaling regulates PGC numbers and motility in organ culture. Mech Dev 124:68–77
Dustin AP (1910) L’origine et l’évolution des gonocytes chez les reptiles. Arch Biol 25:495–534
Everett NB (1945) The present status of the germ cell problem in vertebrates. Biol Rev Camb Philos Soc 20:45–55
Felix W (1911) Die Entwicklung der Harm- und Geschlechtsorgane. In: Keibel-Mall Handbuch der Entwicklungageschichte des Menschen, vol 2. Hirzel, Leipzig, pp 732–955
Fox N, Damjanov I, Martinez-Hernandez A, Knowel BB, Solter D (1981) Immunohistochemical localization of the early embryonic antigen (SSEA-1) in postimplantation mouse embryos and fetal and adult tissue. Dev Biol 83:391–398
Fujiwara Y, Komiya T, Kawabata H, Sato M, Fujimoto H, Furusawa M, Noce T (1994) Isolation of a DEAD-family protein gene that encodes a murine homolog of Drosophila vasa and its specific expression in germ cell lineage. Proc Natl Acad Sci U S A 91:12258–12262
Fuss A (1911) Uber extraregionare Geschlechtszellen bei einem menschlichen Embryo von 4 Wochen. Anat Am 39:407–409
Gamo H (1961) On the origin of germ cells and formation of gonad primordia in the medaka, Olyzias latipes. J Zool 13:101–115
Ginsburg M (1997) Primordial germ cell development in avians. Poult Sci 76:91–95
Ginsburg M, Snow MHL, Mc Laren A (1990) Primordial germ cells in the mouse embryo during gastrulation. Development 110:521–528
Gu Y, Runyan C, Shoemaker A, Surani A, Wylie C (2006) Steel factor controls primordial germ cell survival and motility from the time of their specification in the allantois, and provides a continuous niche throughout their migration. Development 136:1295–1303
Hahnel AC, Eddy EM (1986) Cell surface markers of mouse primordial germ cells defined by two monoclonal antibodies. Gamete Res 15:1235–1244
Hargitt GT (1925) The formation of the sex glands and germ cells of mammals. J Morph Physiol 40:517–557
Haupt A, Joberty G, Bantscheff M, Frohlich H, Stehr H, Schweiger MR, Fischer A, Kerick M, Boerno ST, Dahl A, Lappe M, Lehrach H, Gonzalez C, Drewes G, Lange BMH (2012) Hsp90 inhibition differentially destabilizes MAP linase and TGF-beta signaling components in cancer cells revealed by kinase-targeted chemoproteomics. BMC Cancer 12:38–50
Heys F (1931) The problem of the origin of germ cells. Q Rev Biol 6:1–45
Kazama-Wakabayashi M, Yamaha E, Yamazaki F (1999) The elimination and duplication of lower part of blastoderm effects on the number of primordial germ cells in goldfish. Fish Sci 65:577–582
Koyasu S, Nishida E, Kodawaki T, Matsuzaki F, Lida K, Harada F, Kasuga M, Sakai H, YaharaTwo I (1986) Mammalian heat shock proteins, HSP90 and HSP100, are actin-binding proteins. Proc Natl Acad Sci U S A 83:8054–8058
Lasko PF, Ashburner M (1988) The product of the Drosophila gene vasa is very similar to eukaryotic initiation factor-4A. Nature 335:611–617
Lawson KA, Ray Dunn N, Roelen BAJ, Zeinstra LM, Davis AM, Wright CVE, Korving JPWFM, Hogan BLM (1999) Bmp4 is required for the generation of primordial germ cells in the mouse embryo. Genes Dev 13:424–436
Lejong M, Choa-Duterre M, Vanmuylder N, Louryan S (2018) Geldanamycin administration reduces the amount of primordial germ cells in the mouse embryo. Morphologie 102: 219-224. https://doi.org/10.1016/JMorpho.2018.05.001
Lin TY, Bear M, Du Z, Foley KP, Ying W, Barsoum J, London C (2008) The novel HSP90 inhibitor STA-9090 exhibits activity against Kit-dependent and -independent malignant mast cell tumors. Exp Hematol 36:1266–1277
Louryan S, Evrard L, Glineur R, Vanmuylder N (2002) Protéines de choc thermique, embryogenèse et évolution. Bull Mem Acad R Med Belg 157:293–299
Louryan S, Vanmuylder N, Lambot MA, Rooze M (2003) HSP86: un rôle dans l’évolution humaine ? Anthropol Praehist 114:1–5
Machev N, Fuhrmann G, Viville S (2004) Ontogénèse des cellules germinales primordiales. Med Sci 20:1091–1095
McKay D, Hertig AT, Adams EC, Danziger S (1953) Histochemical observations on the germ cells of human embryos. Anat Rec 17:201–219
McLaren A (2003) Primordial germ cells in the mouse. Dev Biol 262:1–15
Miyata A, Yahara I (1992) The 90-kDa heat shock protein, HSP90, binds and protects casein kinase II from self-aggregation and enhances its kinase activity. J Biol Chem 7:7042–7047
Molyneaux K, Wylie C (2004) Primordial germ cell migration. Int J Dev Biol 48:537–544
Nagai T, Yamaha E, Arai K (2001) Histological differentiation of primordial germ cells in zebrafish. Zool Sci 18:215–223
Neckers L, Workman P (2012) Hsp90 molecular chaperone inhibitors: are we there yet? Clin Cancer Res 18:64–76
Niewkoop D, Sutasurya LA (1979) Primordial germ cells in the chordates. Cambridge University Press, Cambridge
Noce T, Okamoto-Ito S, Tsunekawa N (2001) Vasa homolog genes in mammalian germ cell development. Cell Struct Funct 26:131–136
Olsen LC, Aasland R, Fjose A (1997) A vasa-like gene in zebrafish identifies putative primordial germ cells. Mech Dev 66:95–105
Peuβ R, Eggert H, Armitage SAO, Kurtz J (2015) Downregulation of the evolutionary capacitor Hsp90 is mediated by social cues. Proc R Soc B 282:20152041. https://doi.org/10.1098/rspb.2015.2041
Pfeiffer J, Tarbashevich K, Bandemer J, Palm T, Raz E (2018) Rapid progression through the cell cycle ensures efficient migration of primordial germ cells-the role of Hsp90. Dev Biol 436:84–93
Queitsch C, Sangster TA, Lindquist S (2002) Hsp9O as a capacitor of phenotypic variation. Nature 417:618–624
Rohner N, Jarosz DF, Kowalko JE, Yoshizawa M, Jeffery WR, Borowsky RL, Lindquist S, Tabin CJ (2013) Cryptic variations on morphological evolution: HSP90 as a capacitor for loss of eyes in cavefish. Science 342:1372–1375
Rutherford SL, Lindquist S (1998) Hsp90 as a capacitor for morphological evolution. Nature 396:336–342
Ryan CP, Brownlie JC, Whyard S (2016) Hsp90 and physiological stress are linked to antonomous transposon mobility and heritable genetic change in nematodes. Genome Biol Evol 8:3794–3805
Saitou M, Yamaji M (2012) Primordial germ cells in mice. Cold Spring Harb Perspect Biol 4:1–19
Shevinsky LH, Knowles BB, Damjanov I, Solter D (1982) Monoclonal antibody to murine embryos defines a stage-specific embryonic antigen expressed on mouse embryos and human teratocarcinoma cells. Cell 30:697–705
Simkins CS (1923) Origin and migration of the so-called primordial germ cells in the mouse and rats. Acta Zool 4:241–278
Simkins CS (1928) Origin of sex cells in man. Am J Anat 41:249–272
Sollars V, Lu X, Wang S, Garfinkel MD, Ruden DM (2003) Evidence for an epigenetic mechanism by which Hsp90 acts as a capacitor for morphological evolution. Nat Genet 33:70–74
de Sousa Lopes SM, Roelen BA, Monteiro RM, Emmens R, Lin HY, Li E, Lawson KA, Mummery CL (2004) BMP signaling mediated by ALK2 in the visceral endoderm is necessary for the generation of primordial germ cells in the mouse embryo. Genes Dev 18:1838–1849
Stankiewicz M, Mayer MP (2012) The universe of Hsp90. Biol Mol Concepts 3:79–97
Stebler J, Spieler D, Slanchev K, Molyneaux K, Richter U, Cojocaru V, Tarabykin V, Wylie C, Kessel M, Raz E (2004) Primordial germ cell migration in the chick and mouse embryo: the role of the chemokine SDF-1/CXCL12. Dev Biol 272:351–361
Swift CH (1914) Origin and early history of the primordial germ-cells in the chick. Am J Anat 15:483–516
Taiyab A, Rao CM (2011) Hsp90 modulates actin dynamics: inhibition of Hsp90 leads to decreased cell motility and impairs invasion. Biochim Biophys Acta 1813:213–221
Takeuchi T, Tanigawa Y, Minamide R, Ikenishi K, Komiya T (2010) Analysis of SDF-1/CXCR4 signaling in primordial germ cell migration and survival or differentiation in Xenopus laevis. Mech Dev 27:146–158
Tam PP, Zhou SX (1996) The allocation of epiblast cells to ectodermal and germ-line lineages is influenced by the position of the cells in the gastrulating mouse embryo. Dev Biol 178:124–132
Terayama K, Kataoka K, Morichika K, Orii H, Watanabe K, Mochii M (2013) Developmental regulation of locomotive activity in Xenopus primordial germ cells. Develop Growth Differ 55:217–228
Timmermans LPM (1996) Origin and differentiation of primordial germ cells in vertebrates, especially fishes. Neth J Zool 46:147–162
Tsunekawa N, Naito M, Sakai Y, Nishida T, Noce T (2000) Isolation of chicken vasa homolog gene and tracing the origin of primordial germ cells. Development 127:2741–2750
Urven LE, Erickson CA, Abbott UK, McCarrey JR (1988) Analysis of germ line development in the chick embryo using an anti-mouse EC cell antibody. Development 103:299–304
Vanmuylder N, Evrard L, Daelemans P, Dourov N (2000) Chaperones in the parotid gland: localization of heat shock proteins in human salivary glands. Cells Tissues Organs 167:199–205
Vanmuylder N, Werry-Huet A, Rooze M, Louryan S (2002) Heat shock protein HSP86 expression during mouse embryo development, especially in the germ-line. Anat Embryol 205:301–306
Vanmuylder N, Lambot M-A, Rooze M, Noël J-C, Louryan S (2004) HSP86, cellules germinales at yolk sac tumor. Ann Pathol 24:473–475
Vanmuylder N, Larbi H, Choa-Duterre M, Salvia P, Rooze M, Louryan S (2009) Geldanamycin administration reduces the number of HSP86-positive germ cells in the mouse embryo: preliminary results. Rev Med Brux 30:23–27
Wagner GP, Chiu CH, Hansen TF (1999) Is Hsp90 a regulator of evolvability? J Exp Zool 285:116–118
Wan YQ, Zhang XM, Wang XD, Wang BJ, Wang W (2010) 17-AAG, a Hsp90 inhibitor attenuates the hypoxia induced expression of SDF-1α and ILK in mouse RPE cells. Mol Biol Rep 37:1203–1209
Wang G, Gu X, Chen L, Wang Y, Cao B, E Q (2013) Comparison of the expression of 5 heat shock proteins in benign and malignant salivary gland tumor tissues. Oncol Lett 5:1363–1369
Wu J, Liu T, Rios Z, Mei Q, Lin X, Cao S (2017) Heat shock proteins and cancer. Trends Pharmacol Sci 38:226–256
Yahara I (1999) The role of HSP90 in evolution. Gene Cells 4:375–379
Ying Y, Zhao GQ (2001) Cooperation of endoderm-derived BMP2 and extraembryonic ectoderm-derived BMP4 in primordial germ cell generation in the mouse. Dev Biol 232:484–492
Ying Y, Liu XM, Marble A, Lawson KA, Zhao GQ (2000) Requirement of Bmp8b for the generation of primordial germ cells in the mouse. Mol Endocrinol 14:1053–1063
Yon N, Akbulut C (2015) Identification of primordial germ cells: cytological, histological and immunohistochemical aspects. Braz Arch Biol Technol 58:222–228
Acknowledgements
The authors thank Mrs. M. Choa-Duterre for histological sections.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2019 Springer Nature Switzerland AG
About this chapter
Cite this chapter
Lejong, M., Vanmuylder, N., Louryan, S. (2019). Hsp90 in the Migration of Primordial Germ Cells: A Model to Study Long-Distance Cell Migration and Perhaps Cancer?. In: Asea, A., Kaur, P. (eds) Heat Shock Protein 90 in Human Diseases and Disorders. Heat Shock Proteins, vol 19. Springer, Cham. https://doi.org/10.1007/978-3-030-23158-3_4
Download citation
DOI: https://doi.org/10.1007/978-3-030-23158-3_4
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-030-23157-6
Online ISBN: 978-3-030-23158-3
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)