Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Detection of cross-sex chimerism in the common marmoset monkey (Callithrix jacchus) in interphase cells using fluorescence in situ hybridisation probes specific for the marmoset X and Y chromosomes

E. Wedi A E H , S. Müller B , M. Neusser B , P. H. Vogt C , O. Y. Tkachenko A F , J. Zimmer C , D. Smeets D , H. W. Michelmann G and P. L. Nayudu A
+ Author Affiliations
- Author Affiliations

A Department of Reproductive Biology, German Primate Centre, Goettingen, 37077, Germany.

B Institute of Human Genetics, University Hospital, Ludwig-Maximilians-University Munich, 80336 Munich, Germany.

C Reproduction Genetics Unit, Department of Gynaecological Endocrinology and Reproductive Medicine, University of Heidelberg, 69047, Germany.

D Institute for Anthropology and Human Genetics, Department Biology II, Biocenter, Ludwig-Maximilians-University Munich, 82152 Planegg-Martinsried, Germany.

E Departments of Gastroenterology and Endoscopy, Novel Hôpital Civil (NHC), University Hospital Strasbourg, 67000, France.

F Division of Reproductive & Developmental Sciences, Oregon National Primate Research Center, Oregon Health & Science University, 505 NW 185th Avenue, Beaverton, OR 97006, USA.

G Department of Obstetrics and Gynecology, University of Goettingen, Goettingen, 37075, Germany.

H Corresponding author. Email: edris.wedi@chru-strasbourg.fr

Reproduction, Fertility and Development 29(5) 913-920 https://doi.org/10.1071/RD15321
Submitted: 6 August 2015  Accepted: 19 December 2015   Published: 15 February 2016

Abstract

Chimerism associated with placental sharing in marmosets has been traditionally analysed using conventional chromosome staining on metaphase spreads or polymerase chain reaction. However, the former technique requires the presence of proliferating cells, whereas the latter may be associated with possible blood cell contamination. Therefore, we aimed to develop a single-cell analysis technique for sexing marmoset cells. We applied fluorescent in situ hybridisation (FISH) to cell nuclei using differentially labelled X and Y chromosome-specific probes. Herein we present the validation of this method in metaphase cells from a marmoset lymphoblastoid cell line, as well as application of the method for evaluation of cross-sex chimerism in interphase blood lymphocytes and haematopoietic bone marrow cells from marmosets of same- and mixed-sex litters. The results show conclusively that haematopoietic cells of bone marrow and leucocytes from blood are cross-sex chimeric when the litter is mixed sex. In addition, single samples of liver and spleen cell suspensions from one individual were tested. Cross-sex chimerism was observed in the spleen but not in liver cells. We conclude that FISH is the method of choice to identify cross-sex chimerism, especially when combined with morphological identification of nuclei of different cell types, which will allow a targeted tissue-specific analysis.

Additional keywords: bone marrow cells, lymphocytes.


References

Aeckerle, N., Drummer, C., Debowski, K., Viebahn, C., and Behr, R. (2015). Primordial germ cell development in the marmoset monkey as revealed by pluripotency factor expression: suggestion of a novel model of embryonic germ cell translocation. Mol. Hum. Reprod. 21, 66–80.
Primordial germ cell development in the marmoset monkey as revealed by pluripotency factor expression: suggestion of a novel model of embryonic germ cell translocation.CrossRef | 1:STN:280:DC%2BC2M7jtVaisA%3D%3D&md5=c47dc9c673e544afbfeb975c604bd881CAS | 25237007PubMed | open url image1

Benirschke, K., and Brownhill, L. E. (1962). Further observations on marrow chimerism in marmosets. Cytogenetics 1, 245–257.
Further observations on marrow chimerism in marmosets.CrossRef | 1:STN:280:DyaF387mt1aqsw%3D%3D&md5=7f9d0454bf775eb5c73b0d7d37919fd0CAS | 13970508PubMed | open url image1

Benirschke, K., and Driscoll, S. G. (1967). ‘Pathology of the Human Placenta.’ 1st edn. (Springer-Verlag: New York.)

Benirschke, K., and Layton, W. (1969). An early twin blastocyst of the golden lion marmoset, Leontocebus rosalia L. Folia Primatol. (Basel) 10, 131–138.
An early twin blastocyst of the golden lion marmoset, Leontocebus rosalia L.CrossRef | 1:STN:280:DyaF1M3lvF2rtQ%3D%3D&md5=7f0b53d2378e5ff42f17cefe857efef6CAS | 4979356PubMed | open url image1

Chambers, P. L., and Hearn, J. P. (1985). Embryonic, foetal and placental development in the common marmoset monkey (Callithrix jacchus). J. Zool. 207, 545–561.
Embryonic, foetal and placental development in the common marmoset monkey (Callithrix jacchus).CrossRef | open url image1

Choi, D. H., Kwon, H., Lee, S. D., Moon, M. J., Yoo, E. G., Lee, K. H., Hong, Y. K., and Kim, G. (2013). Testicular hypoplasia in monochorionic dizygous twin with confined blood chimerism. J. Assist. Reprod. Genet. 30, 1487–1491.
Testicular hypoplasia in monochorionic dizygous twin with confined blood chimerism.CrossRef | 24091545PubMed | open url image1

Cremer, T., Landegent, J., Bruckner, A., Scholl, H. P., Schardin, M., Hager, H. D., Devilee, P., Pearson, P., and van der Ploeg, M. (1986). Detection of chromosome aberrations in the human interphase nucleus by visualization of specific target DNAs with radioactive and non-radioactive in situ hybridization techniques: diagnosis of trisomy 18 with probe L1.84. Hum. Genet. 74, 346–352.
Detection of chromosome aberrations in the human interphase nucleus by visualization of specific target DNAs with radioactive and non-radioactive in situ hybridization techniques: diagnosis of trisomy 18 with probe L1.84.CrossRef | 1:STN:280:DyaL2s%2FotF2mtg%3D%3D&md5=432831970f9ebc3fb541794350037fc4CAS | 3793097PubMed | open url image1

Cremer, T., Lichter, P., Borden, J., Ward, D. C., and Manuelidis, L. (1988). Detection of chromosome aberrations in metaphase and interphase tumor cells by in situ hybridization using chromosome-specific library probes. Hum. Genet. 80, 235–246.
Detection of chromosome aberrations in metaphase and interphase tumor cells by in situ hybridization using chromosome-specific library probes.CrossRef | 1:STN:280:DyaL1M%2Fltlejtw%3D%3D&md5=04982ccad4b371a30139eace64c2acc3CAS | 3192213PubMed | open url image1

Delimitreva, S., Wedi, E., Bakker, J., Tkachenko, O. Y., Nikolova, V., and Nayudu, P. L. (2013). Numerical chromosome disorders in the common marmoset (Callithrix jacchus): comparison between two captive colonies. J. Med. Primatol. 42, 177–185.
Numerical chromosome disorders in the common marmoset (Callithrix jacchus): comparison between two captive colonies.CrossRef | 1:STN:280:DC%2BC3srms1Cnsg%3D%3D&md5=8cb4757492ce3be01fcf53f1a06b5c9eCAS | 23600894PubMed | open url image1

Fereydouni, B., Drummer, C., Aeckerle, N., Schlatt, S., and Behr, R. (2014). The neonatal marmoset monkey ovary is very primitive exhibiting many oogonia. Reproduction 148, 237–247.
The neonatal marmoset monkey ovary is very primitive exhibiting many oogonia.CrossRef | 1:CAS:528:DC%2BC2cXht1GgurvI&md5=48c1181a729eea04c8ad60c77c031257CAS | 24840529PubMed | open url image1

Gengozian, N., Batson, J. S., and Eide, P. (1964). Hematologic and cytogenic evidence for chimerism in the marmoset, Tamarinus nigricollis. Sam-Tdr-64-61. AMD TR Rep. Nov, 1–10. open url image1

Gengozian, N., Batson, J. S., Greene, C. T., and Gosslee, D. G. (1969). Hemopoietic chimerism in imported and laboratory-bred marmosets. Transplantation 8, 633–652.
Hemopoietic chimerism in imported and laboratory-bred marmosets.CrossRef | 1:STN:280:DyaE3M7mtFGnsA%3D%3D&md5=3bf5bf9e88f1d9626d022c3609dc26adCAS | 4994820PubMed | open url image1

Gilchrist, R. B., Nayudu, P. L., and Hodges, J. K. (1997). Maturation, fertilization, and development of marmoset monkey oocytes in vitro. Biol. Reprod. 56, 238–246.
Maturation, fertilization, and development of marmoset monkey oocytes in vitro.CrossRef | 1:CAS:528:DyaK2sXislWlsw%3D%3D&md5=57c8159dc52779657bdbd9d241fff272CAS | 9002655PubMed | open url image1

Hearn, J. P. (2001). Embryo implantation and embryonic stem cell development in primates. Reprod. Fertil. Dev. 13, 517–522.
Embryo implantation and embryonic stem cell development in primates.CrossRef | 1:STN:280:DC%2BD383lvFyrsQ%3D%3D&md5=25c752091f9daa399f20dfb372364c99CAS | 11999301PubMed | open url image1

Isachenko, E. F., Nayudu, P. L., Isachenko, V. V., Nawroth, F., and Michelmann, H. W. (2002). Congenitally caused fused labia in the common marmoset (Callithrix jacchus). J. Med. Primatol. 31, 350–355.
Congenitally caused fused labia in the common marmoset (Callithrix jacchus).CrossRef | 1:STN:280:DC%2BD3s%2FhtlKqsA%3D%3D&md5=4748fc1ce837facbe60a997fbc1ba924CAS | 12519214PubMed | open url image1

John, H. A., Birnstiel, M. L., and Jones, K. W. (1969). RNA–DNA hybrids at the cytological level. Nature 223, 582–587.
RNA–DNA hybrids at the cytological level.CrossRef | 1:CAS:528:DyaF1MXltF2ltr4%3D&md5=4adbd3ac797478ae3be026f20e984c2bCAS | 5799530PubMed | open url image1

Kowalzick, L., Artlett, C. M., Thoss, K., Baum, H. P., Ziegler, H., Mischke, D., Blum, R., Ponnighaus, J. M., and Quietzsch, J. (2005). Chronic graft-versus-host-disease-like dermopathy in a child with CD4+ cell microchimerism. Dermatology 210, 68–71.
Chronic graft-versus-host-disease-like dermopathy in a child with CD4+ cell microchimerism.CrossRef | 15604551PubMed | open url image1

Marmoset Genome Sequencing and Analysis Consortium (2014). The Marmoset Genome Sequencing and Analysis Consortium. The common marmoset genome provides insight into primate biology and evolution. Nat. Genet. 46, 850–857.
The Marmoset Genome Sequencing and Analysis Consortium. The common marmoset genome provides insight into primate biology and evolution.CrossRef | 25038751PubMed | open url image1

McLaren, A. (1976). ‘Mammalian Chimaeras.’ (Cambridge University Press: Cambridge.)

Mitchell, R. T., Cowan, G., Morris, K. D., Anderson, R. A., Fraser, H. M., McKenzie, K. J., Wallace, W. H., Kelnar, C. J., Saunders, P. T., and Sharpe, R. M. (2008). Germ cell differentiation in the marmoset (Callithrix jacchus) during fetal and neonatal life closely parallels that in the human. Hum. Reprod. 23, 2755–2765.
Germ cell differentiation in the marmoset (Callithrix jacchus) during fetal and neonatal life closely parallels that in the human.CrossRef | 1:CAS:528:DC%2BD1cXhsVWmt77F&md5=26db950f38715e4522df1d29370b7322CAS | 18694875PubMed | open url image1

Moore, H. D., Gems, S., and Hearn, J. P. (1985). Early implantation stages in the marmoset monkey (Callithrix jacchus). Am. J. Anat. 172, 265–278.
Early implantation stages in the marmoset monkey (Callithrix jacchus).CrossRef | 1:STN:280:DyaL2M7ps1SmsA%3D%3D&md5=2640d7523926fd25c7878134b9461226CAS | 3922211PubMed | open url image1

Neusser, M., Stanyon, R., Bigoni, F., Wienberg, J., and Muller, S. (2001). Molecular cytotaxonomy of New World monkeys (Platyrrhini): comparative analysis of five species by multi-color chromosome painting gives evidence for a classification of Callimico goeldii within the family of Callitrichidae. Cytogenet. Cell Genet. 94, 206–215.
Molecular cytotaxonomy of New World monkeys (Platyrrhini): comparative analysis of five species by multi-color chromosome painting gives evidence for a classification of Callimico goeldii within the family of Callitrichidae.CrossRef | 1:CAS:528:DC%2BD38XhtlGlsbc%3D&md5=4df149d0e70dbb63d35cc1719a9733c1CAS | 11856883PubMed | open url image1

Neusser, M., Schubel, V., Koch, A., Cremer, T., and Muller, S. (2007). Evolutionarily conserved, cell type and species-specific higher order chromatin arrangements in interphase nuclei of primates. Chromosoma 116, 307–320.
Evolutionarily conserved, cell type and species-specific higher order chromatin arrangements in interphase nuclei of primates.CrossRef | 17318634PubMed | open url image1

Padula, A. M. (2005). The freemartin syndrome: an update. Anim. Reprod. Sci. 87, 93–109.
The freemartin syndrome: an update.CrossRef | 1:STN:280:DC%2BD2M3ks1ChtQ%3D%3D&md5=0794b4837aaa8caf6dca7f957980cf36CAS | 15885443PubMed | open url image1

Pardue, M. L., and Gall, J. G. (1970). Chromosomal localization of mouse satellite DNA. Science 168, 1356–1358.
Chromosomal localization of mouse satellite DNA.CrossRef | 1:CAS:528:DyaE3cXksFemtbk%3D&md5=cbd81419aa31144d24d1425357f4f254CAS | 5462793PubMed | open url image1

Pinkel, D., Landegent, J., Collins, C., Fuscoe, J., Segraves, R., Lucas, J., and Gray, J. (1988). Fluorescence in situ hybridization with human chromosome-specific libraries: detection of trisomy 21 and translocations of chromosome 4. Proc. Natl Acad. Sci. USA 85, 9138–9142.
Fluorescence in situ hybridization with human chromosome-specific libraries: detection of trisomy 21 and translocations of chromosome 4.CrossRef | 1:CAS:528:DyaL1MXovFykuw%3D%3D&md5=a70962e48818cc3fbf823d4e0ad39e4fCAS | 2973607PubMed | open url image1

Plohl, M., Mestrovic, N., and Mravinac, B. (2012). Satellite DNA evolution. Genome Dyn. 7, 126–152.
Satellite DNA evolution.CrossRef | 1:CAS:528:DC%2BC38Xhs1GiurzI&md5=2aac0a8156ed355068559a7aff538c51CAS | 22759817PubMed | open url image1

Rohen, J. W., and Lütjen-Drecoll, E. (2002). ‘Funktionelle Embryologie: Die Entwicklung der Funktionssysteme des menschlichen Organismus.’ (Schattauer: Stuttgart.)

Ross, C. N., French, J. A., and Orti, G. (2007). Germ-line chimerism and paternal care in marmosets (Callithrix kuhlii). Proc. Natl. Acad. Sci. USA 104, 6278–6282.
Germ-line chimerism and paternal care in marmosets (Callithrix kuhlii).CrossRef | 1:CAS:528:DC%2BD2sXks1aru7w%3D&md5=08a6b14ff60f1805ca8bdf57405af732CAS | 17389380PubMed | open url image1

Sherlock, J. K., Griffin, D. K., Delhanty, J. D., and Parrington, J. M. (1996). Homologies between human and marmoset (Callithrix jacchus) chromosomes revealed by comparative chromosome painting. Genomics 33, 214–219.
Homologies between human and marmoset (Callithrix jacchus) chromosomes revealed by comparative chromosome painting.CrossRef | 1:CAS:528:DyaK28Xis1ensb4%3D&md5=1ee21d34988280e544370e31823f4508CAS | 8660970PubMed | open url image1

Solovei, I., Grasser, F., and Lanctot, C. (2007). FISH on histological sections. CSH Protoc. 2007, pdb.prot4729.
FISH on histological sections.CrossRef | 21357074PubMed | open url image1

Souter, V. L., Parisi, M. A., Nyholt, D. R., Kapur, R. P., Henders, A. K., Opheim, K. E., Gunther, D. F., Mitchell, M. E., Glass, I. A., and Montgomery, G. W. (2007). A case of true hermaphroditism reveals an unusual mechanism of twinning. Hum. Genet. 121, 179–185.
A case of true hermaphroditism reveals an unusual mechanism of twinning.CrossRef | 17165045PubMed | open url image1

Sweeney, C. G., Curran, E., Westmoreland, S. V., Mansfield, K. G., and Vallender, E. J. (2012). Quantitative molecular assessment of chimerism across tissues in marmosets and tamarins. BMC Genomics 13, 98.
Quantitative molecular assessment of chimerism across tissues in marmosets and tamarins.CrossRef | 22429831PubMed | open url image1

The ENCODE Project Consortium (2007). Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 447, 799–816.
Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project.CrossRef | 17571346PubMed | open url image1

Vabres, P., and Bonneau, D. (2005). Childhood dermatosis due to microchimerism. Dermatology 211, 388–389.
Childhood dermatosis due to microchimerism.CrossRef | 16286760PubMed | open url image1

Wolff, D. J., Bagg, A., Cooley, L. D., Dewald, G. W., Hirsch, B. A., Jacky, P. B., Rao, K. W., Rao, P. N., Association for Molecular Pathology Clinical Practice Committee, and American College of Medical Genetics Laboratory Quality Assurance Committee (2007). Guidance for fluorescence in situ hybridization testing in hematologic disorders. J. Mol. Diagn. 9, 134–143.
Guidance for fluorescence in situ hybridization testing in hematologic disorders.CrossRef | 1:CAS:528:DC%2BD2sXlt12rtbw%3D&md5=30901a1356c899562dcde2616a3bb1e1CAS | 17384204PubMed | open url image1



Rent Article (via Deepdyve) Export Citation

View Altmetrics