Developmental Biology

a worm

Publications

Papers

2017

Schmidt R, Fielmich LE, Grigoriev I, Katrukha EA, Akhmanova A, van den Heuvel S Two populations of cytoplasmic dynein contribute to spindle positioning in C. elegans embryos J Cell Biol. 2017 Jul 24

Amendola PG, Zaghet N, Ramalho JJ, Vilstrup Johansen J, Boxem M, Salcini AE. JMJD-5/KDM8 regulates H3K36me2 and is required for late steps of homologous recombination and genome integrity. PLoS Genet. 2017 Feb 16;13(2).

van Rijnberk LM, van der Horst SE, van den Heuvel S, Ruijtenberg S. A dual transcriptional reporter and CDK-activity sensor marks cell cycle entry and progression in C. elegans.a> PLoS ONE 2017 Feb 12(2)

2016

Portegijs V, Fielmich LE, Galli M, Schmidt R, Muñoz J, van Mourik T, Akhmanova A, Boxem M van den Heuvel S Multisite Phosphorylation of NuMA-Related LIN-5 Controls Mitotic Spindle Positioning in C. elegans. PloS Genetics 2016 Oct 6;12(10)

Van der Vaart A, van den Heuvel S Switching on regeneration. Stem Cell Investigation. 2016;3:41

Waaijers S, Muñoz J, Berends C, Ramalho JJ, Goerdayal SS, Low TY, Zoumaro-Djayoon AD, Hoffmann M, Koorman T, Roderick PT, Harterink M, Seelk S, Kerver J, Hoogenraad CC, Bossinger O, Tursun B, van den Heuvel S, Heck AJR, Boxem M A tissue-specific protein purification approach in Caenorhabditis elegans identifies novel interaction partners of DLG-1/Discs large. BMC Biology 2016 Aug; 14:66

Akhmanova A and van den Heuvel S Tipping the spindle into the right position. JCB. 2016 May;213:293-95.

Koorman T, Klompstra D, van der Voet M, Lemmens I, Ramalho JJ, Nieuwenhuize S, van den Heuvel S, Tavernier J, Nance J, Boxem M. A combined binary interaction and phenotypic map of C. elegans cell polarity proteins. Nat Cell Biol.. 2016 Mar;18(3):337-46.

Harterink M, van Bergeijk P, Allier C, de Haan B, van den Heuvel S, Hoogenraad CC, Kapitein LC. Light-controlled intracellular transport in Caenorhabditis elegans. Curr Biol.. 2016 Feb 22;26(4):R153-4.

Ruijtenberg S, van den Heuvel S. Coordinating cell proliferation and differentiation: Antagonism between cell cycle regulators and cell type-specific gene expression. Cell Cycle. 2016 Jan 17;15(2):196-212.

Chen L, Chuang M, Koorman T, Boxem M, Jin Y, Chisholm AD. Axon injury triggers EFA-6 mediated destabilization of axonal microtubules via TACC and doublecortin like kinase. Elife. 2015 Sep 4;4.

2015

Ruijtenberg S, van den Heuvel S. G1/S Inhibitors and the SWI/SNF Complex Control Cell-Cycle Exit during Muscle Differentiation. Cell. 2015 Jul 16;162(2):300-13.

van Schendel R, Roerink SF, Portegijs V, van den Heuvel S, Tijsterman M. Polymerase Θ is a key driver of genome evolution and of CRISPR/Cas9-mediated mutagenesis. Nat. Commun. 2015 Jun 16;6:7394.

Maia AF, Tanenbaum ME, Galli M, Lelieveld D, Egan DA, Gassmann R, Sunkel CE, van den Heuvel S, Medema RH. Genome-wide RNAi screen for synthetic lethal interactions with the C. elegans kinesin-5 homolog BMK-1. Sci. Data. 2015 May 12;2:150020.

Waaijers S, Ramalho JJ, Koorman T, Kruse E, Boxem M. The C. elegans Crumbs family contains a CRB3 homolog and is not essential for viability. Biol. Open. 2015 Feb 6.

The I, Ruijtenberg S, Bouchet BP, Cristobal A, Prinsen MB, van Mourik T, Koreth J, Xu H, Heck AJ, Akhmanova A, Cuppen E, Boxem M, Muñoz J, van den Heuvel S. Rb and FZR1/Cdh1 determine CDK4/6-cyclin D requirement in C. elegans and human cancer cells. Nat. Commun. 2015 Jan 6;6:5906.

2014

Sapir A, Tsur A, Koorman T, Ching K, Mishra P, Bardenheier A, Podolsky L, Bening-Abu-Shach U, Boxem M, Chou TF, Broday L, Sternberg PW. Controlled sumoylation of the mevalonate pathway enzyme HMGS-1 regulates metabolism during aging. Proc. Natl. Acad. Sci. U.S.A.. 2014 Sep 16;111(37):E3880-9.

de Albuquerque BF, Luteijn MJ, Cordeiro Rodrigues RJ, van Bergeijk P, Waaijers S, Kaaij LJ, Klein H, Boxem M, Ketting RF. PID-1 is a novel factor that operates during 21U-RNA biogenesis in Caenorhabditis elegans. Genes Dev. 2014 Apr 1;28(7):683-688.

Waaijers S, Boxem M. Engineering the Caenorhabditis elegans genome with CRISPR/Cas9. Methods. 2014 Mar 28.

2013

Wang Z, Hou Y, Guo X, van der Voet M, Boxem M, Dixon JE, Chisholm AD, Jin Y. The EBAX-type Cullin-RING E3 Ligase and Hsp90 Guard the Protein Quality of the SAX-3/Robo Receptor in Developing Neurons. Neuron. 2013 Sep 4;79(5):903-16.

Waaijers S, Portegijs V, Kerver J, Lemmens BB, Tijsterman M, van den Heuvel S, Boxem M. CRISPR/Cas9-Targeted Mutagenesis in Caenorhabditis elegans. Genetics. 2013 Aug 26.

*Waaijers S, *Koorman T, Kerver J, Boxem M. Identification of Human Protein Interaction Domains using an ORFeome-based Yeast Two-hybrid Fragment Library. J. Proteome Res. 2013 Jul 5;12(7):3181-92.
*These authors contributed equally

Berends CW, Muñoz J, Portegijs V, Schmidt R, Grigoriev I, Boxem M, Akhmanova A, Heck AJ, van den Heuvel S. F-actin asymmetry and the endoplasmic reticulum-associated TCC-1 protein contribute to stereotypic spindle movements in the Caenorhabditis elegans embryo. Mol Biol. Cell 2013 Jul;24(14):2201-15.

Melo M, Andersson E, Fjelldal PG, Bogerd J, Franca L, Taranger GL, Schulz RW. Salinity and photoperiod modulate pubertal development in Atlantic salmon (Salmo salar). J. Endocrinol. 2013 Dec; in press.

Morais RD, Nóbrega RH, Gómez-González NE, Schmidt R, Bogerd J, França LR, Schulz RW. Thyroid hormone stimulates the proliferation of Sertoli cells and single type A spermatogonia in adult zebrafish (Danio rerio) testis. Endocrinology. 2013 Nov;154(11): 4365-76.

Andersson E, Schulz RW, Male R, Bogerd J, Patiña D, Benedet S, Norgberg B, Taranger GL. Pituitary gonadotropin and ovarian gonadotropin receptor transcript levels: Seasonal and photoperiod-induced changes in the reproductive physiology of female Atlantic salmon (Salmo salar). Gen. Comp. Endocrinol. 2013 Sep;191:247-58.

Baudiffier D, Hinfray N, Ravaud C, Creusot N, Chadili E, Porcher JM, Schulz RW, Brion F. Effect of in vivo chronic exposure to clotramizol on zebrafish testis function. Environ. Sci. Pollut. Res. Int. 2013 May;20(5): 2747-60.

Chen SX, Bogerd J, Schoonen NE, Martijn J, de Waal PP, Schulz RW. A progestin (17a,20b-dihydroxy-4-pregnen-3-one) stimulates early stages of spermatogenesis in zebrafish. Gen. Comp. Endocrinol. 2013 May;185:1-9.

Shao YT, Arvidsson M, Trombley S, Schulz RW, Schmitz M, Borg B. Androgen feedback effects on LH and FSH, and photoperiodic control of reproduction in male three-spined sticklebacks, Gasterosteus aculeatus. Gen. Comp. Endocrinol. 2013 Feb;182:16-23.

Hinfray N, Nóbrega RH, Caulier M, Baudiffier D, Maillot-Maréchal E, Chadili E, Palluel O, Porcher J-M, Schulz RW, Brion F. Cyp17a1 and Cyp19a1 in the zebrafish testis are differentially affected by œstradiol. J. Endocrinol. 2013 Feb;216(3):375-88.

2012

Good S, Yegorov S, Martijn J, Franck J, Bogerd J. New insights into ligand-receptor pairing and coevolution of relaxin family peptides and their receptors in teleosts. Int. J. Evol. Biol. 2012;2012:310278.

Chen SX, Almeida FFL, Andersson E, Taranger GL, Schmidt R, Schulz RW, Bogerd J. Cloning, pharmacological characterization and expression analysis of Atlantic cod (Gadus morhua, L.) nuclear progesterone receptor. Gen. Comp. Endocrinol. 2012 Oct;179(1):71-7.

Baudiffier D, Hinfray N, Vosges M, Creusot N, Chadili E, Porcher JM, Schulz RW, Brion F. A critical role of follicle-stimulating hormone (Fsh) in mediating the effect of clotrimazole on testicular steroidogenesis in adult zebrafish. Toxicology. 2012 Aug;298(1-3): 30-9.

Haugen T, Almeida FF, Andersson E, Bogerd J, Male R, Skaar KS, Schulz RW, Sørhus E, Wijgerde T, Taranger GL. Sex differentiation in Atlantic cod (Gadus morhua L.): morphological and gene expression studies. Reprod. Biol. Endocrinol. 2012 Jun;10:47 (http://www.rbej.com/content/10/1/47 ).

Schulz RW, van Dijk W, Chaves-Pozo E, García-López A, de Franca LR, Bogerd J. Sertoli cell proliferation in the adult testis is induced by unilateral gonadectomy in African catfish. Gen. Comp. Endocrinol. 2012 May;177(1):160-7.

Shao YT, Schulz RW, Borg B. Homeostasis of circulating androgens levels in the breeding male three-spined stickleback (Gasterosteus aculeatus). Zool. Sci. 2012; 51(8):1282-9.

2011

Hinfray N, Baudiffier D, Leal MC, Porcher JM, Aït-Aïssa S, Le Gac F, Schulz RW, Brion F. Characterization of testicular expression of P450 17α-hydroxylase, 17,20-lyase in zebrafish and its perturbation by the pharmaceutical fungicide clotrimazole. Gen. Comp. Endocrinol. 2011 Dec;174(3):309-17.

Korzelius J, The I, Ruijtenberg S, Prinsen MB, Portegijs V, Middelkoop TC, Groot Koerkamp MJ, Holstege FC, Boxem M, van den Heuvel S. Caenorhabditis elegans cyclin D/CDK4 and cyclin E/CDK2 induce distinct cell cycle re-entry programs in differentiated muscle cells. PLoS Genet. 2011 Nov;7(11)

Wildwater M, Sander N, de Vreede G, van den Heuvel S. Cell shape and Wnt signaling redundantly control the division axis of C. elegans epithelial stem cells. Development. 2011 Oct;138(20):4375-85.

Galli M, Muñoz J, Portegijs V, Boxem M, Grill SW, Heck AJ, van den Heuvel S. aPKC phosphorylates NuMA-related LIN-5 to position the mitotic spindle during asymmetric division. Nat. Cell Biol. 2011 Aug 21;13(9):1132-8.

Mukhtar MS, Carvunis AR, Dreze M, Epple P, Steinbrenner J, Moore J, Tasan M, Galli M, Hao T, Nishimura MT, Pevzner SJ, Donovan SE, Ghamsari L, Santhanam B, Romero V, Poulin MM, Gebreab F, Gutierrez BJ, Tam S, Monachello D, Boxem M, Harbort CJ, McDonald N, Gai L, Chen H, He Y; European Union Effectoromics Consortium, Vandenhaute J, Roth FP, Hill DE, Ecker JR, Vidal M, Beynon J, Braun P, Dangl JL. Independently evolved virulence effectors converge onto hubs in a plant immune system network. Science. 2011 Jul 29;333(6042):596-601.

Skaar KS, Nóbrega RH, Magaraki A, Olsen LC, Schulz RW, Male R. Proteolytically activated, recombinant anti-mullerian hormone inhibits androgen secretion, proliferation, and differentiation of spermatogonia in adult zebrafish testis organ cultures. Endocrinology. 2011 Sep;152(9):3527-40.

de Almeida FF, Andersson E, Mittelholzer C, Karlsen O, Taranger GL, Schulz RW. Pituitary gonadotropin and testicular gonadotropin receptor expression in Atlantic cod (Gadusmorhua L.) during the first reproductive season: Effects of photoperiod modulation. Gen. Comp. Endocrinol. 2011 Aug 1;173(1):111-9.

Chen SX, Bogerd J, Andersson E, Almeida FF, Taranger GL, Schulz RW. Cloning, pharmacological characterization, and expression analysis of Atlantic salmon (Salmo salar L.) nuclear progesterone receptor. Reproduction. 2011 Apr;141(4):491-500.

Korzelius J, The I, Ruijtenberg S, Portegijs V, Xu H, Horvitz HR, van den Heuvel S. C. elegans MCM-4 is a general DNA replication and checkpoint component with an epidermis-specific requirement for growth and viability. Dev. Biol. 2011 Feb 15;350(2):358-69.

2010

Nóbrega RH, Greebe CD, van de Kant H, Bogerd J, de França LR, Schulz RW. Spermatogonial stem cell niche and spermatogonial stem cell transplantation in zebrafish. PLoS One. 2010 Sep 20;5(9). pii: e12808.

Angelova K, de Jonge H, Granneman JC, Puett D, Bogerd J. Functional differences of invariant and highly conserved residues in the extracellular domain of the glycoprotein hormone receptors. J. Biol. Chem. 2010 Nov 5;285(45):34813-27.

Kops GJ, van der Voet M, Manak MS, van Osch MH, Naini SM, Brear A, McLeod IX, Hentschel DM, Yates JR 3rd, van den Heuvel S, Shah JV. APC16 is a conserved subunit of the anaphase-promoting complex/cyclosome. J. Cell Sci. 2010 May 15;123(Pt 10):1623-33.

García-López A, de Jonge H, Nóbrega RH, de Waal PP, van Dijk W, Hemrika W, Taranger GL, Bogerd J, Schulz RW. Studies in zebrafish reveal unusual cellular expression patterns of gonadotropin receptor messenger ribonucleic acids in the testis and unexpected functional differentiation of the gonadotropins. Endocrinology. 2010 May;151(5):2349-60.

Chen SX, Bogerd J, García-López A, de Jonge H, de Waal PP, Hong WS, Schulz RW. Molecular cloning and functional characterization of a zebrafish nuclear progesterone receptor. Biol. Reprod. 2010 Jan;82(1):171-81.

Levavi-Sivan B, Bogerd J, Mañanós EL, Gómez A, Lareyre JJ. Perspectives on fish gonadotropins and their receptors. Gen. Comp. Endocrinol. 2010 Feb 1;165(3):412-37.

Taranger GL, Carrillo M, Schulz RW, Fontaine P, Zanuy S, Felip A, Weltzien FA, Dufour S, Karlsen O, Norberg B, Andersson E, Hansen T. Control of puberty in farmed fish. Gen. Comp. Endocrinol. 2010 Feb 1;165(3):483-515.

Schulz RW, de França LR, Lareyre JJ, Le Gac F, Chiarini-Garcia H, Nobrega RH, Miura T. Spermatogenesis in fish. Gen. Comp. Endocrinol. 2010 Feb 1;165(3):390-411.

2009

Good-Avila SV, Yegorov S, Harron S, Bogerd J, Glen P, Ozon J, Wilson BC. Relaxin gene family in teleosts: phylogeny, syntenic mapping, selective constraint, and expression analysis. BMC Evol. Biol. 2009 Dec 16;9:293.

Dreze M, Charloteaux B, Milstein S, Vidalain PO, Yildirim MA, Zhong Q, Svrzikapa N, Romero V, Laloux G, Brasseur R, Vandenhaute J, Boxem M, Cusick ME, Hill DE, Vidal M. 'Edgetic' perturbation of a C. elegans BCL2 ortholog. Nat. Methods. 2009 Nov;6(11):843-9.

van der Voet M, Lorson MA, Srinivasan DG, Bennett KL, van den Heuvel S. C. elegans mitotic cyclins have distinct as well as overlapping functions in chromosome segregation. Cell Cycle. 2009 Dec 15;8(24):4091-102.

Sillé FC, Boxem M, Sprengers D, Veerapen N, Besra G, Boes M. Distinct requirements for CD1d intracellular transport for development of Vα14 iNKT cells. J. Immunol. 2009 Aug 1;183(3):1780-8.

Stetak A, Hörndli F, Maricq AV, van den Heuvel S, Hajnal A. Neuron-specific regulation of associative learning and memory by MAGI-1 in C. elegans. PLoS One. 2009 Jun 24;4(6):e6019.

Andersson E, Nijenhuis W, Male R, Swanson P, Bogerd J, Taranger GL, Schulz RW. Pharmacological characterization, localization and quantification of expression of gonadotropin receptors in Atlantic salmon (Salmo salar L.) ovaries. Gen. Comp. Endocrinol. 2009 Sep 15;163(3):329-39.

de Waal PP, Leal MC, García-López A, Liarte S, de Jonge H, Hinfray N, Brion F, Schulz RW, Bogerd J. Oestrogen-induced androgen insufficiency results in a reduction of proliferation and differentiation of spermatogonia in the zebrafish testis. J. Endocrinol. 2009 Aug;202(2):287-97.

Leal MC, Cardoso ER, Nóbrega RH, Batlouni SR, Bogerd J, França LR, Schulz RW. Histological and stereological evaluation of zebrafish (Danio rerio) spermatogenesis with an emphasis on spermatogonial generations. Biol. Reprod. 2009 Jul;81(1):177-87.

Leal MC, de Waal PP, García-López A, Chen SX, Bogerd J, Schulz RW. Zebrafish primary testis tissue culture: an approach to study testis function ex vivo. Gen. Comp. Endocrinol. 2009 Jun;162(2):134-8.

van der Voet M, Berends CW, Perreault A, Nguyen-Ngoc T, Gönczy P, Vidal M, Boxem M, van den Heuvel S. NuMA-related LIN-5, ASPM-1, calmodulin and dynein promote meiotic spindle rotation independently of cortical LIN-5/GPR/Gα. Nat. Cell Biol. 2009 Mar;11(3):269-77.

Simonis N, Rual JF, Carvunis AR, Tasan M, Lemmens I, Hirozane-Kishikawa T, Hao T, Sahalie JM, Venkatesan K, Gebreab F, Cevik S, Klitgord N, Fan C, Braun P, Li N, Ayivi-Guedehoussou N, Dann E, Bertin N, Szeto D, Dricot A, Yildirim MA, Lin C, de Smet AS, Kao HL, Simon C, Smolyar A, Ahn JS, Tewari M, Boxem M, Milstein S, Yu H, Dreze M, Vandenhaute J, Gunsalus KC, Cusick ME, Hill DE, Tavernier J, Roth FP, Vidal M. Empirically controlled mapping of the Caenorhabditis elegans protein-protein interactome network. Nat. Methods. 2009 Jan;6(1):47-54.

Almeida FF, Taranger GL, Norberg B, Karlsen O, Bogerd J, Schulz RW. Photoperiod-modulated testis maturation in Atlantic cod (Gadus morhua, L.). Biol. Reprod. 2009 Apr;80(4):631-40.

García-López A, Bogerd J, Granneman JC, van Dijk W, Trant JM, Taranger GL, Schulz RW. Leydig cells express follicle-stimulating hormone receptors in African catfish. Endocrinology. 2009 Jan;150(1):357-65.

2008

van den Heuvel S, Dyson NJ. Conserved functions of the pRB and E2F families. Nat. Rev. Mol. Cell Biol. 2008 Sep;9(9):713-24.

Galli M, van den Heuvel S. Determination of the cleavage plane in early C. elegans embryos. Annu. Rev. Genet. 2008 Vol. 42:389-411.

Komatsu H, Chao MY, Larkins-Ford J, Corkins ME, Somers GA, Tucey T, Dionne HM, White JQ, Wani K, Boxem M, Hart AC. OSM-11 facilitates LIN-12 Notch signaling during Caenorhabditis elegans vulval development. PLoS Biol. 2008 Aug 12;6(8):e196.

Boxem M, Maliga Z, Klitgord N, Li N, Lemmens I, Mana M, de Lichtervelde L, Mul JD, van de Peut D, Devos M, Simonis N, Yildirim MA, Cokol M, Kao HL, de Smet AS, Wang H, Schlaitz AL, Hao T, Milstein S, Fan C, Tipsword M, Drew K, Galli M, Rhrissorrakrai K, Drechsel D, Koller D, Roth FP, Iakoucheva LM, Dunker AK, Bonneau R, Gunsalus KC, Hill DE, Piano F, Tavernier J, van den Heuvel S, Hyman AA, Vidal M. A protein domain-based interactome network for C. elegans early embryogenesis. Cell. 2008 Aug 8;134(3):534-45.

de Waal PP, Wang DS, Nijenhuis WA, Schulz RW, Bogerd J. Functional characterization and expression analysis of the androgen receptor in zebrafish (Danio rerio) testis. Reproduction. 2008 Aug;136(2):225-34.

Vischer HF, Granneman JC, Koelink PJ, Marques RB, Bogerd J. Identification of a luteinizing hormone-selective determinant in the exodomain of a follicle-stimulating hormone receptor. Gen. Comp. Endocrinol. 2008 May 1;156(3):490-8.

van Bragt MP, Roepers-Gajadien HL, Korver CM, Bogerd J, Okuda A, Eggen BJ, de Rooij DG, van Pelt AM. Expression of the pluripotency marker UTF1 is restricted to a subpopulation of early A spermatogonia in rat testis. Reproduction. 2008 Jul;136(1):33-40.

Schulz RW, Liemburg M, García-López A, Dijk W, Bogerd J. Androgens modulate testicular androgen production in African catfish (Clarias gariepinus) depending on the stage of maturity and type of androgen. Gen. Comp. Endocrinol. 2008 Mar 1;156(1):154-63.

Leal MC, Feitsma H, Cuppen E, França LR, Schulz RW. Completion of meiosis in male zebrafish (Danio rerio) despite lack of DNA mismatch repair gene mlh1. Cell Tissue Res. 2008 Apr;332(1):133-9.

Clayton JE, van den Heuvel SJ, Saito RM. Transcriptional control of cell-cycle quiescence during C. elegans development. Dev. Biol. 2008 Jan 15;313(2):603-13.

Almeida FF, Kristoffersen C, Taranger GL, Schulz RW. Spermatogenesis in Atlantic cod (Gadus morhua): a novel model of cystic germ cell development. Biol Reprod. 2008 Jan;78(1):27-34.

2007

Schulz RW, Bogerd J, Male R, Ball J, Fenske M, Olsen LC, Tyler CR. Estrogen-induced alterations in amh and dmrt1 expression signal for disruption in male sexual development in the zebrafish. Environ. Sci. Technol. 2007 Sep 1;41(17):6305-10.

Korzelius J, van den Heuvel S. Replication licensing: oops! ... I did it again. Curr. Biol. 2007 Aug 21;17(16):R630-2.

Zmora N, Kazeto Y, Kumar RS, Schulz RW, Trant JM. Production of recombinant channel catfish (Ictalurus punctatus) FSH and LH in S2 Drosophila cell line and an indication of their different actions. J. Endocrinol. 2007 Aug;194(2):407-16.

Dasgupta U, Dixit BL, Rusch M, Selleck S, The I. Functional conservation of the human EXT1 tumor suppressor gene and its Drosophila homolog tout velu. Dev. Genes Evol. 2007 Aug;217(8):555-61.

Wildwater M, The I, van den Heuvel S. Coordination of cell proliferation and differentiation: finding a GEM in the root? Dev. Cell. 2007 Jun;12(6):841-2.

Mizrak SC, Renault-Mihara F, Párraga M, Bogerd J, van de Kant HJ, López-Casas PP, Paz M, del Mazo J, de Rooij DG. Phosphoprotein enriched in astrocytes-15 is expressed in mouse testis and protects spermatocytes from apoptosis. Reproduction. 2007 Apr;133(4):743-51.

Su VF, Jones KA, Brodsky M, The I. Quantitative analysis of Hedgehog gradient formation using an inducible expression system. BMC Dev. Biol. 2007 May 7;7:43.

Ceron J, Rual JF, Chandra A, Dupuy D, Vidal M, van den Heuvel S. Large-scale RNAi screens identify novel genes that interact with the C. elegans retinoblastoma pathway as well as splicing-related components with synMuv B activity. BMC Dev. Biol. 2007 Apr 6;7:30.

Feitsma H, Leal MC, Moens PB, Cuppen E, Schulz RW. Mlh1 deficiency in zebrafish results in male sterility and aneuploid as well as triploid progeny in females. Genetics. 2007 Apr;175(4):1561-9.

Bogerd J. Ligand-selective determinants in gonadotropin receptors. Mol. Cell. Endocrinol. 2007 Jan 2;260-262:144-52.

Dijkstra PD, Hekman R, Schulz RW, Groothuis TGG. Social stimulation, nuptial colouration, androgens and immunocompetence in a sexual dimorphic cichlid fish. Behav. Ecol. Sociobiol. 2007 Vol. 61, 599-609.

Rehbein H, Bogerd J. Identification of genetically modified zebrafish (Danio rerio) by protein- and DNA-analysis. Journal of Consumer Protection and Food Safety. 2007 Vol. 2, 122-125.

2006

Mizrak SC, Bogerd J, Lopez-Casas PP, Párraga M, Del Mazo J, de Rooij DG. Expression of stress inducible protein 1 (Stip1) in the mouse testis. Mol. Reprod. Dev. 2006 Nov;73(11):1361-6.

Yang F, Vought BW, Satterlee JS, Walker AK, Jim Sun ZY, Watts JL, DeBeaumont R, Saito RM, Hyberts SG, Yang S, Macol C, Iyer L, Tjian R, van den Heuvel S, Hart AC, Wagner G, Näär AM. An ARC/Mediator subunit required for SREBP control of cholesterol and lipid homeostasis. Nature. 2006 Aug 10;442(7103):700-4.

Boxem M. Cyclin-dependent kinases in C. elegans. Cell Div. 2006 May 12;1:6.

Vischer HF, Granneman JC, Bogerd J. Identification of follicle-stimulating hormone-selective beta-strands in the N-terminal hormone-binding exodomain of human gonadotropin receptors. Mol. Endocrinol. 2006 Aug;20(8):1880-93.

Navratil AM, Farmerie TA, Bogerd J, Nett TM, Clay CM. Differential impact of intracellular carboxyl terminal domains on lipid raft localization of the murine gonadotropin-releasing hormone receptor. Biol. Reprod. 2006 May;74(5):788-97.

Shirayama M, Soto MC, Ishidate T, Kim S, Nakamura K, Bei Y, van den Heuvel S, Mello CC. The Conserved Kinases CDK-1, GSK-3, KIN-19, and MBK-2 Promote OMA-1 Destruction to Regulate the Oocyte-to-Embryo Transition in C. elegans. Curr. Biol. 2006 Jan 10;16(1):47-55.

Schulz RW, Andersson E, Taranger GL. Photoperiod manipulation can stimulate or inhibit pubertal testis maturation in Atlantic salmon (Salmo salar). Anim. Reprod. 2006 Vol. 3, 121-126.

2005

Bogerd J. Selective ligand-binding determinants in catfish and human gonadotropin receptors. Fish Physiol. Biochem. 2005 Apr;31(2-3):247-54.

Raghuveer K, Garhwal R, Wang DS, Bogerd J, Kirubagaran R, Rasheeda MK, Sreenivasulu G, Bhattachrya N, Tarangini S, Nagahama Y, Senthilkumaran B. Effect of methyl testosterone- and ethynyl estradiol-induced sex differentiation on catfish, Clarias gariepinus: expression profiles of DMRT1, Cytochrome P450 aromatases and 3 beta-hydroxysteroid dehydrogenase. Fish Physiol. Biochem. 2005 Apr;31(2-3):143-7.

Rual JF, Venkatesan K, Hao T, Hirozane-Kishikawa T, Dricot A, Li N, Berriz GF, Gibbons FD, Dreze M, Ayivi-Guedehoussou N, Klitgord N, Simon C, Boxem M, Milstein S, Rosenberg J, Goldberg DS, Zhang LV, Wong SL, Franklin G, Li S, Albala JS, Lim J, Fraughton C, Llamosas E, Cevik S, Bex C, Lamesch P, Sikorski RS, Vandenhaute J, Zoghbi HY, Smolyar A, Bosak S, Sequerra R, Doucette-Stamm L, Cusick ME, Hill DE, Roth FP, Vidal M. Towards a proteome-scale map of the human protein-protein interaction network. Nature. 2005 Oct 20;437(7062):1173-8.

Schulz RW, Menting S, Bogerd J, França LR, Vilela DA, Godinho HP. Sertoli cell proliferation in the adult testis—evidence from two fish species belonging to different orders. Biol. Reprod. 2005 Nov;73(5):891-8.

Bogerd J, Granneman JC, Schulz RW, Vischer HF. Fish FSH receptors bind LH: how to make the human FSH receptor to be more fishy? Gen. Comp. Endocrinol. 2005 May 15;142(1-2):34-43.

Koreth J, van den Heuvel S. Cell-cycle control in Caenorhabditis elegans: how the worm moves from G1 to S. Oncogene. 2005 Apr 18;24(17):2756-64.

van den Heuvel S. The C. elegans cell cycle: overview of molecules and mechanisms. Methods Mol. Biol. 2005 Vol. 296:51-67.

2004

Dupuy D, Li QR, Deplancke B, Boxem M, Hao T, Lamesch P, Sequerra R, Bosak S, Doucette-Stamm L, Hope IA, Hill DE, Walhout AJ, Vidal M. A first version of the Caenorhabditis elegans Promoterome. Genome Res. 2004 Oct;14(10B):2169-75.

Rual JF, Ceron J, Koreth J, Hao T, Nicot AS, Hirozane-Kishikawa T, Vandenhaute J, Orkin SH, Hill DE, van den Heuvel S, Vidal M. Toward improving Caenorhabditis elegans phenome mapping with an ORFeome-based RNAi library. Genome Res. 2004 Oct;14(10B):2162-8.

Boxem M, Tsai CW, Zhang Y, Saito RM, Liu JO. The C. elegans methionine aminopeptidase 2 analog map-2 is required for germ cell proliferation. FEBS Lett. 2004 Oct 8;576(1-2):245-50.

Vischer HF, Marques RB, Granneman JC, Linskens MH, Schulz RW, Bogerd J. Receptor-selective determinants in catfish gonadotropin seat-belt loops. Mol. Cell. Endocrinol. 2004 Sep 30;224(1-2):55-63.

Miley GR, Fantz D, Glossip D, Lu X, Saito RM, Palmer RE, Inoue T, Van Den Heuvel S, Sternberg PW, Kornfeld K. Identification of residues of the Caenorhabditis elegans LIN-1 ETS domain that are necessary for DNA binding and regulation of vulval cell fates. Genetics. 2004 Aug;167(4):1697-709.

Blomenröhr M, Vischer HF, Bogerd J. Receptor mutagenesis strategies for examination of structure-function relationships. Methods Mol. Biol. 2004 Vol. 259:307-22.

Saito RM, Perreault A, Peach B, Satterlee JS, van den Heuvel S. The CDC-14 phosphatase controls developmental cell-cycle arrest in C. elegans. Nat. Cell Biol. 2004 Aug;6(8):777-83.

Zhang H, Christoforou A, Aravind L, Emmons SW, van den Heuvel S, Haber DA. The C. elegans Polycomb gene sop-2 encodes an RNA binding protein. Mol. Cell. 2004 Jun 18;14(6):841-7.

Fisk Green R, Lorson M, Walhout AJ, Vidal M, van den Heuvel S. Identification of critical domains and putative partners for the Caenorhabditis elegans spindle component LIN-5. Mol. Genet. Genomics. 2004 Jun;271(5):532-44.

Zhang H, Smolen GA, Palmer R, Christoforou A, van den Heuvel S, Haber DA. SUMO modification is required for in vivo Hox gene regulation by the Caenorhabditis elegans Polycomb group protein SOP-2. Nat. Genet. 2004 May;36(5):507-11.

Vogelaar CF, Hoekman MF, Brakkee JH, Bogerd J, Burbach JP. Developmental regulation of homeobox gene expression in dorsal root ganglion neurons is not recapitulated during regeneration of the crushed sciatic nerve. Neuroscience. 2004 Vol. 125(3):645-50.

*Vidalain PO, *Boxem M, Ge H, Li S, Vidal M. Increasing specificity in high-throughput yeast two-hybrid experiments. Methods. 2004 Apr;32(4):363-70.
*These authors contributed equally

Tewari M, Hu PJ, Ahn JS, Ayivi-Guedehoussou N, Vidalain PO, Li S, Milstein S, Armstrong CM, Boxem M, Butler MD, Busiguina S, Rual JF, Ibarrola N, Chaklos ST, Bertin N, Vaglio P, Edgley ML, King KV, Albert PS, Vandenhaute J, Pandey A, Riddle DL, Ruvkun G, Vidal M. Systematic interactome mapping and genetic perturbation analysis of a C. elegans TGF-beta signaling network. Mol. Cell. 2004 Feb 27;13(4):469-82.

van den Heuvel S. Protein degradation: CUL-3 and BTB—partners in proteolysis. Curr. Biol. 2004 Jan 20;14(2):R59-61.

*Li S, *Armstrong CM, *Bertin N, *Ge H, *Milstein S, *Boxem M, *Vidalain PO, *Han JD, *Chesneau A, Hao T, Goldberg DS, Li N, Martinez M, Rual JF, Lamesch P, Xu L, Tewari M, Wong SL, Zhang LV, Berriz GF, Jacotot L, Vaglio P, Reboul J, Hirozane-Kishikawa T, Li Q, Gabel HW, Elewa A, Baumgartner B, Rose DJ, Yu H, Bosak S, Sequerra R, Fraser A, Mango SE, Saxton WM, Strome S, Van Den Heuvel S, Piano F, Vandenhaute J, Sardet C, Gerstein M, Doucette-Stamm L, Gunsalus KC, Harper JW, Cusick ME, Roth FP, Hill DE, Vidal M. A map of the interactome network of the metazoan C. elegans. Science. 2004 Jan 23;303(5657):540-3.
*These authors contributed equally

2003

Vischer HF, Granneman JC, Linskens MH, Schulz RW, Bogerd J. Both recombinant African catfish LH and FSH are able to activate the African catfish FSH receptor. J. Mol. Endocrinol. 2003 Aug;31(1):133-40.

Vischer HF, Granneman JC, Bogerd J. Opposite contribution of two ligand-selective determinants in the N-terminal hormone-binding exodomain of human gonadotropin receptors. Mol. Endocrinol. 2003 Oct;17(10):1972-81.

Srinivasan DG, Fisk RM, Xu H, van den Heuvel S. A complex of LIN-5 and GPR proteins regulates G protein signaling and spindle function in C elegans. Genes Dev. 2003 May 15;17(10):1225-39.

Vischer HF, Bogerd J. Cloning and functional characterization of a testicular TSH receptor cDNA from the African catfish (Clarias gariepinus). J. Mol. Endocrinol. 2003 Apr;30(2):227-38.

Teves AC, Granneman JC, van Dijk W, Bogerd J. Cloning and expression of a functional estrogen receptor-alpha from African catfish (Clarias gariepinus) pituitary. J. Mol. Endocrinol. 2003 Apr;30(2):173-85.

Yajnik V, Paulding C, Sordella R, McClatchey AI, Saito M, Wahrer DC, Reynolds P, Bell DW, Lake R, van den Heuvel S, Settleman J, Haber DA. DOCK4, a GTPase activator, is disrupted during tumorigenesis. Cell. 2003 Mar 7;112(5):673-84.

Vischer HF, Teves AC, Ackermans JC, van Dijk W, Schulz RW, Bogerd J. Cloning and spatiotemporal expression of the follicle-stimulating hormone beta subunit complementary DNA in the African catfish (Clarias gariepinus). Biol. Reprod. 2003 Apr;68(4):1324-32.

Okuzawa K, Gen K, Bruysters M, Bogerd J, Gothilf Y, Zohar Y, Kagawa H. Seasonal variation of the three native gonadotropin-releasing hormone messenger ribonucleic acids levels in the brain of female red seabream. Gen. Comp. Endocrinol. 2003 Feb 15;130(3):324-32.

Vischer HF, Granneman JC, Noordam MJ, Mosselman S, Bogerd J. Ligand selectivity of gonadotropin receptors. Role of the beta-strands of extracellular leucine-rich repeats 3 and 6 of the human luteinizing hormone receptor. J. Biol. Chem. 2003 May 2;278(18):15505-13.

Vischer HF, Bogerd J. Cloning and functional characterization of a gonadal luteinizing hormone receptor complementary DNA from the African catfish (Clarias gariepinus). Biol. Reprod. 2003 Jan;68(1):262-71.

Schulz RW, van Dijk W, Bogerd J. Sertoli cell proliferation and FSH signalling in African catfish, Clarias gariepinus. Fish Physiol. Biochem. 2003 Vol. 28, 223-224.

Schulz RW. Endocrine regulation of spermatogenesis in teleost fish. Ann. Rev. Biomed. Sci. 2003 Vol. 5, 57-68.

2002

Blomenröhr M, Bogerd J, Leurs R, Goos H. Differences in structure-function relations between nonmammalian and mammalian GnRH receptors: what we have learnt from the African catfish GnRH receptor. Prog. Brain Res. 2002 Vol. 141:87-93.

Bogerd J, Diepenbroek WB, Hund E, van Oosterhout F, Teves AC, Leurs R, Blomenröhr M. Two gonadotropin-releasing hormone receptors in the African catfish: no differences in ligand selectivity, but differences in tissue distribution. Endocrinology. 2002 Dec;143(12):4673-82.

Lokman PM, Harris B, Kusakabe M, Kime DE, Schulz RW, Adachi S, Young G. 11-Oxygenated androgens in female teleosts: prevalence, abundance, and life history implications. Gen. Comp. Endocrinol. 2002 Oct 15;129(1):1-12.

Legler J, Zeinstra LM, Schuitemaker F, Lanser PH, Bogerd J, Brouwer A, Vethaak AD, De Voogt P, Murk AJ, Van der Burg B. Comparison of in vivo and in vitro reporter gene assays for short-term screening of estrogenic activity. Environ. Sci. Technol. 2002 Oct 15;36(20):4410-5.

Pfleger KD, Bogerd J, Millar RP. Conformational constraint of mammalian, chicken, and salmon GnRHs, but not GnRH II, enhances binding at mammalian and nonmammalian receptors: evidence for preconfiguration of GnRH II. Mol. Endocrinol. 2002 Sep;16(9):2155-62.

Consten D, Keuning ED, Bogerd J, Zandbergen MA, Lambert JG, Komen J, Goos HJ. Sex steroids and their involvement in the cortisol-induced inhibition of pubertal development in male common carp, Cyprinus carpio L. Biol. Reprod. 2002 Aug;67(2):465-72.

Boxem M, van den Heuvel S. C. elegans class B synthetic multivulva genes act in G1 regulation. Curr. Biol. 2002 Jun 4;12(11):906-11.

Rebers FE, Hassing GA, van Dijk W, van Straaten E, Goos HJ, Schulz RW. Gonadotropin-releasing hormone does not directly stimulate luteinizing hormone biosynthesis in male African catfish. Biol. Reprod. 2002 Jun;66(6):1604-11.

Saito RM, van den Heuvel S. Malignant worms: what cancer research can learn from C. elegans. Cancer Invest. 2002 Vol. 20(2):264-75.

Micchelli CA, The I, Selva E, Mogila V, Perrimon N. Rasp, a putative transmembrane acyltransferase, is required for Hedgehog signaling. Development. 2002 Feb;129(4):843-51.

Blomenröhr M, ter Laak T, Kühne R, Beyermann M, Hund E, Bogerd J, Leurs R. Chimaeric gonadotropin-releasing hormone (GnRH) peptides with improved affinity for the catfish (Clarias gariepinus) GnRH receptor. Biochem J. 2002 Feb 1;361(Pt 3):515-23.

Garcia Hernandez MP, Garcia Ayala A, Agulleiro B, Garcia A, van Dijk W, Schulz RW. Development of a homologous radioimmunoassay for Mediterranean yellowtail (Seriola dumerilii, Risso 1810) LH. Aquaculture. 2002 Vol. 210, 203-218.

Viveiros ATM, Fessehaye Y, ter Veld M, Schulz RW, Komen J. Hand-stripping of semen and semen quality after maturational hormone treatments, in African catfish Clarias gariepinus. Aquaculture. 2002 Vol. 213, 373-386.

Schulz RW, Miura T. Spermatogenesis and its endocrine regulation. Fish Physiol. Biochem. 2002 Vol. 26, 43-56.

2001

Cavaco JE, Bogerd J, Goos H, Schulz RW. Testosterone inhibits 11-ketotestosterone-induced spermatogenesis in African catfish (Clarias gariepinus). Biol. Reprod. 2001 Dec;65(6):1807-12.

Boxem M, van den Heuvel S. lin-35 Rb and cki-1 Cip/Kip cooperate in developmental regulation of G1 progression in C. elegans. Development. 2001 Nov;128(21):4349-59.

Wang L, Oh DY, Bogerd J, Choi HS, Ahn RS, Seong JY, Kwon HB. Inhibitory activity of alternative splice variants of the bullfrog GnRH receptor-3 on wild-type receptor signaling. Endocrinology. 2001 Sep;142(9):4015-25.

Dubois EA, Zandbergen MA, Peute J, Bogerd J, Goos HJ. Development of three distinct GnRH neuron populations expressing two different GnRH forms in the brain of the African catfish (Clarias gariepinus). J. Comp. Neurol. 2001 Aug 27;437(3):308-20.

Blomenröhr M, Kühne R, Hund E, Leurs R, Bogerd J, ter Laak T. Proper receptor signalling in a mutant catfish gonadotropin-releasing hormone receptor lacking the highly conserved Asp(90) residue. FEBS Lett. 2001 Jul 20;501(2-3):131-4.

Schulz RW, Vischer HF, Cavaco JE, Santos EM, Tyler CR, Goos HJ, Bogerd J. Gonadotropins, their receptors, and the regulation of testicular functions in fish. Comp. Biochem. Physiol. B. Biochem. Mol. Biol. 2001 Jun;129(2-3):407-17.

Bogerd J, Blomenröhr M, Andersson E, van der Putten HH, Tensen CP, Vischer HF, Granneman JC, Janssen-Dommerholt C, Goos HJ, Schulz RW. Discrepancy between molecular structure and ligand selectivity of a testicular follicle-stimulating hormone receptor of the African catfish (Clarias gariepinus). Biol. Reprod. 2001 Jun;64(6):1633-43.

Cavaco JE, van Baal J, van Dijk W, Hassing GA, Goos HJ, Schulz RW. Steroid hormones stimulate gonadotrophs in juvenile male African catfish (Clarias gariepinus). Biol. Reprod. 2001 May;64(5):1358-65.

Hu B, Mitra J, van den Heuvel S, Enders GH. S and G2 phase roles for Cdk2 revealed by inducible expression of a dominant-negative mutant in human cells. Mol. Cell Biol. 2001 Apr;21(8):2755-66.

Consten D, Bogerd J, Komen J, Lambert JG, Goos HJ. Long-term cortisol treatment inhibits pubertal development in male common carp, Cyprinus carpio L. Biol. Reprod. 2001 Apr;64(4):1063-71.

Bosma PT, Blázquez M, Fraser EJ, Schulz RW, Docherty K, Trudeau VL. Sex steroid regulation of glutamate decarboxylase mRNA expression in goldfish brain is sexually dimorphic. J. Neurochem. 2001 Feb;76(4):945-56.

Wang L, Yoo MS, Kang HM, Im WB, Choi HS, Bogerd J, Kwon HB. Cloning and characterization of cDNAs encoding the GnRH1 and GnRH2 precursors from bullfrog (Rana catesbeiana). J. Exp. Zool. 2001 Feb 15;289(3):190-201.

Wang L, Bogerd J, Choi HS, Seong JY, Soh JM, Chun SY, Blomenröhr M, Troskie BE, Millar RP, Yu WH, McCann SM, Kwon HB. Three distinct types of GnRH receptor characterized in the bullfrog. Proc. Natl. Acad. Sci. USA. 2001 Jan 2;98(1):361-6.

Mikolajczyk T, Roelants I, Epler R, Ollevier F, Schulz RW, Sokolowska-Mikolajczyk M, Breton B. Assessment of tissue damaging effects of mixed micellar absorption enhancers on the intestinal mucosa of common carp (Cyprinus carpio), African catfish (Clarias gariepinus) and rainbow trout (Oncorhynchus mykiss) as a consequence of enhanced intestinal absorption of sGnRH-a. J. Appl. Ichthyol. 2001 Vol. 17, 267-272.

2000

The I, Perrimon N. Morphogen diffusion: the case of the wingless protein. Nat. Cell Biol. 2000 May;2(5):E79-82.

1999

The I, Bellaiche Y, Perrimon N. Hedgehog movement is regulated through tout velu-dependent synthesis of a heparan sulfate proteoglycan. Mol. Cell. 1999 Oct;4(4):633-9.

1998

Bellaiche Y, The I, Perrimon N. Tout-velu is a Drosophila homologue of the putative tumour suppressor EXT-1 and is needed for Hh diffusion. Nature. 1998 Jul 2;394(6688):85-8.

1997

Guo HF, The I, Hannan F, Bernards A, Zhong Y. Requirement of Drosophila NF1 for activation of adenylyl cyclase by PACAP38-like neuropeptides. Science. 1997 May 2;276(5313):795-8.

The I, Hannigan GE, Cowley GS, Reginald S, Zhong Y, Gusella JF, Hariharan IK, Bernards A. Rescue of a Drosophila NF1 mutant phenotype by protein kinase A. Science. 1997 May 2;276(5313):791-4.

1995

Ishioka C, Ballester R, Engelstein M, Vidal M, Kassel J, The I, Bernards A, Gusella JF, Friend SH. A functional assay for heterozygous mutations in the GTPase activating protein related domain of the neurofibromatosis type 1 gene. Oncogene. 1995 Mar 2;10(5):841-7.

1993

The I, Murthy AE, Hannigan GE, Jacoby LB, Menon AG, Gusella JF, Bernards A. Neurofibromatosis type 1 gene mutations in neuroblastoma. Nat Genet. 1993 Jan;3(1):62-6.

Book Chapters

Fielmich L-E and Van den Heuvel S. Polarity Control of Spindle Positioning in the C. elegans Embryo. a> In: Cell Polarity in Development and Disease (Volume 2) Springer, Edited by Klaus Ebnet. 2015 Feb. ISBN 978-3-319-14466-5

Van den Heuvel S, Kipreos ET. C. elegans cell cycle analysis. In: Methods Cell Biol. 2012 107:265-94.

Ruijtenberg S, van den Heuvel S, The I. Regulation of DNA synthesis and replication checkpoint activation during C. elegans development. In: Tech Open Access Books. Edited by Jelena Kusic-Tisma. 2011 Sep. ISBN 978-953-307-775-8

Schulz R.W. and Nobrega R.H. (2011) Anatomy and Histology of Fish Testis. In: Farrell A.P., (ed.), Encyclopedia of Fish Physiology: From Genome to Environment, volume 1, pp. 616–626. San Diego: Academic Press

Schulz R.W. and Nobrega R.H. (2011) Regulation of Spermatogenesis. In: Farrell A.P., (ed.), Encyclopedia of Fish Physiology: From Genome to Environment, volume 1, pp. 627–634. San Diego: Academic Press.

van den Heuvel S. Cell-cycle regulation. WormBook. 2005 Sep 21:1-16.

Van den Heuvel S. The C. elegans cell cycle: overview of molecules and mechanisms. In: Methods in Molecular Biology. Edited by G Brooks and T Humphry, Humana Press, Inc. 2004 Vol 296, Cell Cycle Control, Mechanisms and Protocols. 51-67