Isolation, Characterization, and Organ-Specific Expression of Two Novel Human Zinc Finger Genes Related to theDrosophilaGenespalt
Abstract
The region-specific homeotic gene spalt (sal) of Drosophila specifies head and tail as opposed to trunk segments. During later stages of ontogenesis, sal is also expressed and required in a small number of tissues and organs in the developing embryo. sal encodes a zinc finger protein of unusual but characteristic structure. We made use of these unique features to isolate sal-like genes from humans. Here we report the isolation and molecular characterization of two sal-like transcription units, termed Hsal1 and Hsal2, which are located on chromosomes 16q12.1 and 14q11.1-q12.1, respectively. Their transcripts are expressed in a limited number of adult organs, including the brain. While Hsal2 is evenly expressed in different brain areas, Hsal1 transcripts preferentially accumulate in the corpus callosum and the substantia nigra. In the fetal brain, transcripts of both genes were detected in neurons. The arrangement of sal-like zinc finger domains and their high degree of sequence similarity suggest a novel and conserved subfamily of human zinc finger transcription factors that is closely related to the Drosophila gene product encoded by the gene sal.
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Differentiated cell types such as kidney cells, microglia or neurons express high levels of SALL1, 2 and 3.
“differentiated cell types such as kidney cells 57 , microglia 58 or neurons 59 express high levels of SALL1, 2 and 3”
From Tetramerisation governs SALL transcription factor function in development and disease (2025) · cites this paper as [57]
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Mutations in the SALL1 putative transcription factor gene cause Townes-Brocks syndrome
Kohlhase, J., Wischermann, A., Reichenbach, H., Froster, U., & Engel, W. (1998) · Nature Genetics · doi:10.1038/ng0198-81 · Cited by 481 · see citing works
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“Thus, it is the fourth member of a group of human C2H2type zinc finger proteins proposed to encode organ-specific transcription factors closely related to the Drosophila melanogaster spalt (sal) gene (Kohlhase et al. 1996, 1999).”
BackgroundOkihiro syndrome is caused by SALL4 mutations
Kohlhase, J. (2002) · Human Molecular Genetics · doi:10.1093/hmg/11.23.2979 · Cited by 320 · see citing works
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Bmi-1 is a target gene for SALL4 in hematopoietic and leukemic cells
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“The SALL1 protein, however, contains four putative DNA binding domains (Kohlhase et al. 1996), and it remains to be shown which and how many of these are essential for gene function.”
BackgroundSelf-citationInvestigation of meiotic rearrangements in DGS/VCFS patients with a microdeletion 22q11.2
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“Four such genes have been identified, and two of these (SALL2 [Kohlhase et al., 1996] and SALL3 [Kohlhase et al., 1999a]) have not yet been associated with human diseases.”
BackgroundSelf-citationSALL4 is a key regulator of survival and apoptosis in human leukemic cells
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“Vertebrate spalt proteins fall into four groups, with four genes in human called SALL1-4 (Kohlhase et al., 1996, 1999, 2002b).”
BackgroundSALL4 Expression in Gonocytes and Spermatogonial Clones of Postnatal Mouse Testes
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Self-citationSALL3, a new member of the human spalt-like gene family, maps to 18q23.
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“SALL1 and SALL2 encode proteins that contain three distinct DNA-binding zincfinger domains and have primarily been shown to play a role in region specification (Kohlhase et al., 1996).”
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Self-citationRole of SALL4 in the progression and metastasis of colorectal cancer
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“The SALL gene family, including four members (SALL1 to SALL4) was initially cloned based on DNA sequence homology to Drosophila gene spalt (sal) [3].”
MethodSALL4 is directly activated by TCF/LEF in the canonical Wnt signaling pathway
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Self-citationSALL4 as a new biomarker for early colorectal cancers
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“It has two major isoforms named SALL4A and SALL4B (Kohlhase et al. 1996).”
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“SALL1 comprises three exons (Kohlhase et al., 1996; Kohlhase et al., 1998) encoding a zinc finger protein thought to act as a transcriptional repressor (Netzer et al.”
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“…Sall4; Okihiro syndrome; mouse; organogenesis; embryonic stem cells SALL4 is a member of the SALL gene family of zinc finger transcription factors (Kohlhase et al., 1996), containing multiple C2H2 double zinc finger domains, homologous to the Drosophila spalt (sal) homeotic gene important in…”
BackgroundHedgehog Signaling in the Normal and Diseased Pancreas
Kayed, H., Kleeff, J. H., Osman, T., Keleg, S., Büchler, M. W., & Friess, H. (2006) · Pancreas · doi:10.1097/01.mpa.0000202937.55460.0c · Cited by 70 · see citing works
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Stem Cell Gene SALL4 Suppresses Transcription through Recruitment of DNA Methyltransferases
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Enhanced self-renewal of hematopoietic stem/progenitor cells mediated by the stem cell gene Sall4
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Embryonic expression of the murine homologue of SALL1, the gene mutated in Townes--Brocks syndrome.
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Self-citationp150Sal2 Is a p53-Independent Regulator of p21WAF1/CIP
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“Although involvement of off-target mutations in the SALL1 / fetuses cannot be ruled out, possible influence of SALL1-KO in multiple organs/tissues, including brain, limb buds, and heart (Kohlhase et al., 1996; Usui et al., 2012), is more likely the cause of fetal lethality in pigs.”
BackgroundParrish, M., Ott, T., Lance-Jones, C., Schuetz, G., Schwaeger-Nickolenko, A., & Monaghan, A. P. (2004) · Molecular and Cellular Biology · doi:10.1128/mcb.24.16.7102-7112.2004 · Cited by 61 · see citing works
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Transcriptional Activation of the SALL1 by the Human SIX1 Homeodomain during Kidney Development*
Chai, L., Yang, J.-C., Di, C., Cui, W., Kawakami, K., Lai, R., & Ma, Y.-P. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m600180200 · Cited by 53
Congenital anomalies of the kidney and urinary tract: an embryogenetic review.
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Zinc Finger Protein SALL4 Functions through an AT-Rich Motif to Regulate Gene ExpressionPreprint
Kong, N., Bassal, M., Tan, H.-K., Kurland, J. V., Yong, K. J., Young, J. J., Yang, Y., Li, F.-D., Lee, J. D., Liu, Y. J., et al. (2020) · bioRxiv · doi:10.1101/2020.07.03.186783 · Cited by 51 · see citing works
“Spalt-like (SALL) 4 is a transcription factor that is a member of the SALL gene family, the homologs of the Drosophila homeotic gene Spalt, which are conserved throughout eukaryotes [1, 2].”
BackgroundYamashita, K., Sato, A., Asashima, M., Wang, P., & Nishinakamura, R. (2007) · Genes to Cells · doi:10.1111/j.1365-2443.2007.01042.x · Cited by 52 · see citing works
“Humans have four sal homolog genes ( SALL1 , SALL2 , SALL3 and SALL4 ), similar to the case for mice ( Sall1 , Sall2 , Sall3 and Sall4 ) (Kohlhase et al. 1996, 1999, 2000, 2002a,b; Ott et al. 1996, 2001; Buck et al. 2000, 2001; Al-Baradie et al. 2002).”
BackgroundMolecular cloning of a novel Xenopus spalt gene (Xsal-3).
Onuma, Y., Nishinakamura, R., Takahashi, S., Yokota, T., & Asashima, M. (1999) · Biochemical and Biophysical Research Communications - BBRC · doi:10.1006/bbrc.1999.1479 · Cited by 49 · see citing works
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“…aminoterminal part of all known SAL-like proteins (Buck et al., 2000; Farrell and Munsterberg, 2000; Farrell et al., 2001; Hollemann et al., 1996; Kohlhase et al., 2000; Kohlhase et al., 1999a; Kohlhase et al., 1996; Köster et al., 1997; Kühnlein et al., 1994; Onuma et al., 1999; Ott et al., 1996).”
BackgroundMethodInfluentialSelf-citationRegulation of Drosophila spalt gene expression.
Kühnlein, R., Brönner, G., Taubert, H., & Schuh, R. (1997) · Mechanisms of Development · doi:10.1016/s0925-4773(97)00103-2 · Cited by 47
“, mouse (Ott and Schiitz, 1996) and human (Kohlhase et al., 1996).”
BackgroundSelf-citationMutation of SALL2 causes recessive ocular coloboma in humans and mice
Kelberman, D., Islam, L., Lakowski, J., Bacchelli, C., Chanudet, E., Lescai, F., Patel, A., Stupka, E., Buck, A., Wolf, S., et al. (2014) · Human Molecular Genetics · doi:10.1093/hmg/ddt643 · Cited by 46 · see citing works
Self-citationDrosophila spalt/spalt-related mutants exhibit Townes-Brocks' syndrome phenotypes
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“…10 0 50 100 Number of touches % r es po nd in g to a t l ea st n to uc he s wild type sem-4 (n2654) sem-4 (n2087) sem-4 (n1378) sem-4 (n1971) 3839sem-4 represses egl-5 and mec-3 thalamus, which constitutes a very small portion of the entire brain (Kohlhase et al., 1996; Nakagawa and O’Leary, 2001).”
BackgroundZhang, L., Yan, Y., Jiang, Y., Cui, Y., Zou, Y., Qian, J., Luo, C., Lu, Y., & Wu, X. (2014) · Journal of Neuro-Oncology · doi:10.1007/s11060-014-1646-4 · Cited by 45 · see citing works
Genomic cloning, chromosomal mapping, and expression analysis of Msal-2
Kohlhase, J., Altmann, M., Archangelo, L., Dixkens, C., & Engel, W. (2000) · Mammalian Genome · doi:10.1007/s003350010012 · Cited by 45 · see citing works
“Also, in contrast toMsal, Xsal-1,and SALL1, SALL2 does not contain a 38 intron (Kohlhase et al. 1996).”
BackgroundResultInfluentialSelf-citationZinc Finger Protein Sall2 Is Not Essential for Embryonic and Kidney Development
Sato, A., Matsumoto, Y., Koide, U., Kataoka, Y., Yoshida, N., Yokota, T., Asashima, M., & Nishinakamura, R. (2003) · Molecular and Cellular Biology · doi:10.1128/mcb.23.1.62-69.2003 · Cited by 44 · see citing works
SALL4 as a transcriptional and epigenetic regulator in normal and leukemic hematopoiesis
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Expression of Xenopus XlSALL4 during limb development and regeneration
Neff, A. W., King, M. W., Harty, M. W., Nguyen, T., Calley, J. N., Smith, R. C., & Mescher, A. L. (2005) · Developmental Dynamics · doi:10.1002/dvdy.20363 · Cited by 41 · see citing works
“Four human SAL homologues have been identified to date: SALL1 (Kohlhase et al., 1998), SALL2 (Kohlhase et al., 1996), SALL3 (Kohlhase et al., 1999), and SALL4 (Kohlhase et al., 2002a; Al-Baradie et al., 2002).”
BackgroundMa, Y.-P., Li, D.-W., Chai, L., Luciani, A., Ford, D., Morgan, J., & Maizel, A. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m106468200 · Cited by 42 · see citing works
Molecular cloning, chromosomal localization, and expression of the murine SALL1 ortholog Sall1
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“This localization further indicates that Sall1 is orthologous to SALL1 because 8D is homologous to human chromosome 16q, where SALL1 is located (Kohlhase et al., 1996).”
BackgroundSelf-citationLi, D.-W., Dower, K., Ma, Y.-P., Tian, Y., & Benjamin, T. (2001) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.251447198 · Cited by 40 · see citing works
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Miertus, J., Borozdin, W., Frecer, V., Tonini, G., Bertok, S., Amoroso, A., Miertus, S., & Kohlhase, J. (2006) · Human Genetics · doi:10.1007/s00439-005-0124-7 · Cited by 39 · see citing works
“It still remains unclear if mutations in SALL2 (Kohlhase et al. 1996) and SALL3 (Kohlhase et al. 1999) are likewise associated with human malformation syndromes.”
BackgroundSelf-citationOncofetal gene SALL4 and prognosis in cancer: A systematic review with meta-analysis
Nicolè, L., Sanavia, T., Veronese, N., Cappellesso, R., Luchini, C., Dabrilli, P., & Fassina, A. (2017) · Oncotarget · doi:10.18632/oncotarget.14952 · Cited by 39 · see citing works
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Townes-Brocks syndrome and renal dysplasia: a novel mutation in the SALL1 gene
Salerno, A., Kohlhase, J., & Kaplan, B. S. (2000) · Pediatric nephrology (Berlin, West) · doi:10.1007/s004670050006 · Cited by 37 · see citing works
Self-citationSALL Proteins; Common and Antagonistic Roles in Cancer
Álvarez, C., Quiroz, A., Benítez-Riquelme, D., Riffo, E., Castro, A. F., & Pincheira, R. (2021) · Cancers · doi:10.3390/cancers13246292 · Cited by 37 · see citing works
Developmental SALL2 transcription factor: a new player in cancer.
Hermosilla, V., Hepp, M. I., Escobar, D., Farkas, C., Riffo, E., Castro, A. F., & Pincheira, R. (2017) · Carcinogenesis · doi:10.1093/carcin/bgx036 · Cited by 35 · see citing works
Sall3 is required for the terminal maturation of olfactory glomerular interneurons
Harrison, S. J., Parrish, M. E., & Monaghan, A. P. (2008) · The Journal of Comparative Neurology · doi:10.1002/cne.21650 · Cited by 31 · see citing works
“…of four mammalian members of the Sall gene family, which are widely expressed throughout development, in the peripheral and central nervous system as well as in peripheral organs (AlBaradie et al., 2002; Buck et al., 2000, 2001; Kohlhase et al., 1996, 1999, 2000, 2002a,b; Ott et al., 1996, 2001).”
BackgroundEpigenetic control of melanoma cell invasiveness by the stem cell factor SALL4
Diener, J., Baggiolini, A., Pernebrink, M., Dalcher, D., Lerra, L., Cheng, P. F., Varum, S., Häusel, J., Stierli, S., Treier, M., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-25326-8 · Cited by 34 · see citing works
Shuai, X., Zhou, D., Shen, T., Wu, Y., Zhang, J., Wang, X., & Li, Q. (2009) · Cancer Genetics and Cytogenetics · doi:10.1016/j.cancergencyto.2009.06.006 · Cited by 28 · see citing works
SALL1 expression in the human pituitary-adrenal/gonadal axis
Ma, Y., Chai, L., Cortez, S., Stopa, E. G., Mm, S., Ford, D., Morgan, J., & Maizel, A. (2002) · Journal of Endocrinology · doi:10.1677/joe.0.1730437 · Cited by 28 · see citing works
“The predicted transcript codes are 1325 amino acids in length for SALL1 and 1008 amino acids for SALL2, based on translation of the open reading frames (Kohlhase et al. 1996, Ma et al. 2001b; Genbank database accession no.”
BackgroundKohlhase, J., Liebers, M., Backe, J., Baumann-Muller, A., Bembea, M., Destrėe, A., Gattas, M., Grüssner, S., Muller, T., Mortier, G., et al. (2003) · Journal of Medical Genetics · doi:10.1136/jmg.40.11.e127 · Cited by 30 · see citing works
Self-citationDefining the heterochromatin localization and repression domains of SALL1.
Netzer, C., Bohlander, S., Hinzke, M., Chen, Y., & Kohlhase, J. (2006) · Biochimica et Biophysica Acta · doi:10.1016/j.bbadis.2005.12.005 · Cited by 29 · see citing works
Self-citationSynergistic cooperation of Sall4 and Cyclin D1 in transcriptional repression
Böhm, J., Kaiser, F. J., Borozdin, W., Depping, R., & Kohlhase, J. (2007) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2007.03.050 · Cited by 23 · see citing works
Self-citationHsal 1 is related to kidney and gonad development and is expressed in Wilms tumor
Ma, Y., Singer, D. B., Gozman, A., Ford, D., Chai, L., Steinhoff, M. M., Hansen, K., & Maizel, A. (2001) · Pediatric Nephrology · doi:10.1007/s004670100624 · Cited by 25 · see citing works
Functional and clinical significance of SALL4 in breast cancer
Dirican, E., & Akkіprіk, M. (2016) · Tumor Biology · doi:10.1007/s13277-016-5150-7 · Cited by 23 · see citing works
Interaction of the developmental regulator SALL1 with UBE2I and SUMO-1.
Netzer, C., Bohlander, S., Rieger, L., Müller, S., & Kohlhase, J. (2002) · Biochemical and Biophysical Research Communications - BBRC · doi:10.1016/s0006-291x(02)02003-x · Cited by 24
Self-citationCloning and expression of CSAL2, a new member of the spalt gene family in chick.
Farrell, E. R., Tosh, G., Church, E., & Münsterberg, A. (2001) · Mechanisms of Development · doi:10.1016/s0925-4773(01)00296-9 · Cited by 24 · see citing works
“Phylogenetic comparison of all full-length vertebrate Spalt proteins currently isolated (Hollemann et al., 1996; Kohlhase et al., 1996, 1999, 2000; Ott et al., 1996; Koster et al., 1997; Onuma et al., 1999; Farrell and Mu Ènsterberg, 2000) suggests that the Spalt family can be divided into at least…”
Dai, K.-S., & Liew, C.-C. (1999) · Journal of Molecular and Cellular Cardiology · doi:10.1006/jmcc.1999.1011 · Cited by 24
Hermosilla, V., Salgado, G., Riffo, E., Escobar, D., Hepp, M. I., Farkas, C., Galindo, M. A., Morín, V., García-Robles, M., Castro, A. F., et al. (2018) · Molecular Oncology · doi:10.1002/1878-0261.12308 · Cited by 21 · see citing works
“Both isoforms are highly expressed in the brain (Kohlhase et al., 1996, 2000; Ma et al., 2001).”
BackgroundGu, M., Wang, X., Toh, T. B., Hooi, L., Tenen, D. G., & Chow, E. K. (2018) · Advanced Therapeutics · doi:10.1002/adtp.201800110 · Cited by 21 · see citing works
The next new target in leukemia: The embryonic stem cell geneSALL4
Wang, F., Zhao, W., Kong, N. R., Cui, W., & Chai, L. (2014) · Molecular & Cellular Oncology · doi:10.4161/23723548.2014.969169 · Cited by 19 · see citing works
Harrison, S. J., Nishinakamura, R., & Monaghan, A. P. (2007) · Cerebral Cortex · doi:10.1093/cercor/bhm191 · Cited by 22 · see citing works
“Mutation or deletion of these genes in humans is associated with distinct disorders with abnormalities in the limbs, ear, anus, kidney, and heart (Kohlhase et al. 1996, 1999; Al-Baradie et al. 2002; Kohlhase, Heinrich, Schubert, et al. 2002).”
BackgroundRodriguez, E. F., Chen, L., Ao, M.-H., Geddes, S., Gabrielson, E., Askin, F. B., Zhang, H., & Li, Q. K. (2014) · Translational Respiratory Medicine · doi:10.1186/s40247-014-0010-7 · Cited by 20 · see citing works
Faguer, S., Pillet, A., Chassaing, N., Merhenberger, M., Bernadet-Monrozies, P., Guitard, J., & Chauveau, D. (2008) · Nephrology, Dialysis and Transplantation · doi:10.1093/ndt/gfp014 · Cited by 19
“SALL1 is one of the four mammalian homologues of the Drosophila region-specific homeotic gene spalt [6].”
BackgroundExpression of csal1 in pre limb-bud chick embryos
Sweetman, D., Smith, T. G., Farrell, E. R., & Münsterberg, A. (2005) · The International Journal of Developmental Biology · doi:10.1387/ijdb.051985ds · Cited by 13 · see citing works
“A number of orthologues have been identified in Drosophila (Barrio et al., 1996), human (Kohlhase et al., 1996, Kohlhase et al., 1999a, Kohlhase et al., 2002), mouse (Ott et al., 1996, Buck et al., 2000, Kohlhase et al., 2000, Kohlhase et al., 2002), Xenopus (Hollemann et al., 1996, Onuma et al.,…”
BackgroundPowell, C. M., & Michaelis, R. C. (1999) · Journal of Medical Genetics · doi:10.1136/jmg.36.2.89 · Cited by 150 · see citing works
Böhm, J., Munk‐Schulenburg, S., Felscher, S., & Kohlhase, J. (2006) · American Journal of Medical Genetics Part A · doi:10.1002/ajmg.a.31383 · Cited by 19 · see citing works
“Thehuman SALL1 gene encodes aC2H2 zinc finger transcription factor related to SAL from Drosophila melanogaster [Kohlhase et al., 1996].”
BackgroundSelf-citationLiberalesso, P., Cordeiro, M. L., Karuta, S., Koladicz, K., Nitsche, A., Zeigelboim, B., Raskin, S., & Rauchman, M. (2017) · BMC Medical Genetics · doi:10.1186/s12881-017-0483-7 · Cited by 17
Identification and Characterization of Sall1-Expressing Cells Present in the Adult Mouse Kidney
Abedin, M. J., Imai, N., Rosenberg, M. E., & Gupta, S. (2011) · Nephron Experimental Nephrology · doi:10.1159/000328925 · Cited by 16 · see citing works
Sung, C. K., Dahl, J., Yim, H., Rodig, S. J., & Benjamin, A. T. L. (2011) · The FASEB Journal · doi:10.1096/fj.10-173674 · Cited by 18 · see citing works
Subramaniam, M. M., Navarro, S., Pellín, A., López-Guerrero, J., Carda, C., Alvaro, J. A. H., Sabater, P. L. G., & Llombart-Bosch, A. (2006) · Virchows Archiv · doi:10.1007/s00428-006-0271-9 · Cited by 17
- Authors
- Kohlhase, J., Schuh, R., Dowe, G., Kühnlein, R. P., Jäckle, H., Schroeder, B., Schulz-Schaeffer, W., Kretzschmar, H. A., Köhler, A., Müller, U., Raab-Vetter, M., Burkhardt, E., Engel, W., & Stick, R.
- Affiliations
- Max Planck Institute for Biophysical Chemistry (DE)
- University of Göttingen (DE)
- Justus-Liebig-Universität Gießen (DE)
- Corresponding author
- Jäckle, Herbert
- Venue
- Genomics
- Publisher
- Elsevier BV
- Published
- 1996-12
- Volume
- 38
- Issue
- 3
- Pages
- 291-298
- ISSN
- 0888-7543 (ISSN-L)
- OpenAlex
- W1982290479
- Cited by
- 145
- References
- 0
- Citations by year
- 2026: 1 · 2025: 6 · 2024: 1 · 2021: 3 · 2020: 2 · 2019: 2 · 2018: 9 · 2017: 7 · 2016: 4 · 2015: 2 · 2014: 10 · 2013: 5 · 2012: 1
- FWCI
- 1.51
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Genomics (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Deutsche Forschungsgemeinschaft
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
- Keywords
- zinc finger transcription factor, human genes, homeotic genes, organ-specific gene expression, brain expression, corpus callosum, substantia nigra, gene isolation
- MeSH terms
- Adult, Amino Acid Sequence, Animals, Brain, Chromosomes, Human, Pair 14, Chromosomes, Human, Pair 16, Cloning, Molecular, DNA-Binding Proteins, Drosophila melanogaster, Embryonic and Fetal Development, Genes, Humans, Molecular Sequence Data, Nerve Tissue Proteins, Organ Specificity, Species Specificity, Transcription Factors, Transcription, Genetic, Gene Expression, Zinc Fingers, Sequence Alignment, Sequence Homology, Amino Acid, Homeodomain Proteins, Drosophila Proteins
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