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Massive Loss of Mid- and Hindbrain Neurons During Embryonic Development of Homozygous Lurcher Mice

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Massive Loss of Mid- and Hindbrain Neurons During Embryonic Development of Homozygous Lurcher Mice The Journal of Neuroscience, April 1, 1997, 17(7):2400–2407 Massive Loss of Mid- and Hindbrain Neurons during Embryonic Development of Homozygous Lurcher Mice Susie So-Wun Cheng and Nathaniel Heintz Howard Hughes Medical Institute, The Laboratory of Molecular Biology, The Rockefeller University, New York, New York 10021 The mouse neurological mutant lurcher (Lc) results from a embryonic development. A particularly conspicuous conse- semidominant mutation. Heterozygous Lc/1 mice are viable quence of the Lc/Lc genotype at birth is the complete absence but ataxic because Lc/1 Purkinje cells die by apoptosis within of large neurons comprising the trigeminal motor nucleus. the first 3 weeks of life. Lc/Lc mice die shortly after birth. To aid These neurons arise normally and are maintained until E15.5. in understanding the function of the lurcher gene product, we However, beginning at E15.5 large numbers of pyknotic cells have examined the embryonic development of homozygous are evident in the trigeminal motor nucleus, suggesting that lurcher animals. The ratio of 1/1:Lc/1:Lc/Lc animals did not these cells die coincident with their terminal differentiation in deviate significantly from the expected 1:2:1. Homozygous the developing hindbrain. Because the trigeminal motor nu- lurcher mice at P0 were found to be normal under gross mor- cleus controls muscles required for suckling, these results phological examination. However, these mice weighed less, suggest an explanation for the neonatal death of homozygous lacked milk in their stomach, and died within the first day of life. Lc animals. These data demonstrate that the severe and dose- No resorbed embryos were found at embryonic day (E) 17.5, dependent developmental consequences of lurcher gene ac- indicating that all homozygous lurchers survived until birth. tion result from degeneration of distinct neuronal populations Histological examination of P0 animals revealed that in ho- on maturation in the developing CNS. mozygous lurcher mice the patterning of the brain is normal but Key words: cerebellum; lurcher; homozygous phenotype; cell that there has been a massive loss of hindbrain neurons during death; midbrain; hindbrain The semidominant mouse neurological mutant lurcher was de- lurcher phenotype. Systematic studies of these animals have been scribed first by Philips (1960) and later characterized extensively hindered by the lack of reliable genetic markers to genotype by others (Wetts and Herrup, 1982a,b; Heckroth, 1994a,b; Nor- accurately the lurcher animals during embryonic development. To man et al., 1995). Heterozygous lurcher mice are fertile, although gain a better understanding of the action of the Lc gene, we have they have reduced litter size and lower body weight (Wilson, investigated the dose dependence of the Lc phenotype in defini- 1975). Adult Lc animals are ataxic and tend to fall in their tively genotyped developing Lc/Lc animals. We find that survival attempts to walk (Philips, 1960). This results from the complete of homozygous lurcher animals is normal until birth and that all of loss of Lc/1 cerebellar Purkinje cells beginning during the first these animals die within the first day of life. Although gross few postnatal weeks (Sidman et al., 1965). Studies of Lc 7 patterning of the Lc/Lc brain appears normal, in these animals wild-type chimeric mice have shown that Purkinje cell death in there is a massive loss of hindbrain neurons during late embryo- Lc/1 animals is cell-autonomous (Wetts and Herrup, 1982a,b). In genesis. In particular, we note as the first sign of the Lc/Lc both normal and heterozygous lurcher animals, Purkinje cells are genotype the degeneration of the trigeminal motor nucleus, be- born between embryonic days 11 (E11) and 13 (E13) in the ginning with the death of large neurons in this structure between developing cerebellar anlage. Lc/1 Purkinje cells survive in nor- E15.5 and E16.5 and resulting in its complete absence in P0 pups. mal numbers beyond birth, although the entire population even- Because the trigeminal motor nucleus is required for function of tually is lost between postnatal days 8 and 65 (Caddy and Biscoe, the musculature involved in suckling, loss of this structure con- 1979). This is followed by the gradual loss of granule cells in the tributes to the neonatal death of Lc/Lc animals. Furthermore, Lc/1 cerebellum. We recently have shown that Lc/1 Purkinje several striking parallels between Purkinje cell death in Lc/1 cells die by apoptosis and that they begin their final program of animals and motor neuron death in Lc/Lc animals are evident, differentiation before their death as a consequence of lurcher suggesting that the dose dependence of the lurcher phenotype gene action (Norman et al., 1995). results from a differential sensitivity of these neuronal cell types to Despite the extensive studies of the Lc/1 phenotype and the a single essential factor. initial report that lurcher homozygotes probably die shortly after birth (Philips, 1960), very little is known about the homozygous MATERIALS AND METHODS Animal crosses and molecular genotyping. Progeny for intercrosses were Received Oct. 24, 1996; revised Jan. 9, 1997; accepted Jan. 13, 1997. generated by mating M. castaneus with B6CBA-Awj/A-Lc mice, pur- This work was supported by the Howard Hughes Medical Institute. We thank John chased from the Jackson Laboratory (Bar Harbor, ME). F1 animals Gubbay and other members of the Heintz Lab for useful discussions. expressing the lurcher phenotype then were selected and intercrossed. Correspondence should be addressed to Dr. Nathaniel Heintz, Howard Hughes Progeny from the F1 intercross can be genotyped after birth as well as at Medical Institute, The Laboratory of Molecular Biology, The Rockefeller University, various points in gestation. Genomic DNA was isolated from the tail of 1230 York Avenue, New York, NY 10021. mice after birth or from the yolk sac of prenatal mice. Primers MIT-121 Copyright q 1997 Society for Neuroscience 0270-6474/97/172400-08$05.00/0 and MIT-175 that were found to be mapped closely to lurcher (Zuo et al., Cheng and Heintz • Neuronal Loss in lurcher Homozygotes J. Neurosci., April 1, 1997, 17(7):2400–2407 2401 1995) were used in PCR to amplify the M. castaneus allele and B6CBA weights of homozygous lurcher P0 neonates were significantly less allele. The PCR product then was resolved on an 8% acrylamide gel. than their heterozygous and wild-type littermates. Thus, there was Mice that are Lc/Lc have only the B6CBA allele amplified. Lc/1 will have both the M. castaneus and B6CBA alleles amplified, and 1/1 has only the no significant difference in weight between the wild-type and M. castaneus allele amplified. heterozygous neonates (1.21 6 0.18 gm; n 5 16, p . 0.1), whereas Isolation of DNA from embryos and neonates. Days 12.5, 15.5, and 16.5 there was a significant reduction in the average weight of Lc/Lc embryos from heterozygous intercrosses were dissected out of uteri, and pups at the time of birth (1.09 6 0.1 gm; n 5 10; 0.01 . p . the yolk sacs were removed for DNA isolation. The DNA was prepared by incubation in tail buffer (50 mM Tris, pH 8.0, 100 mM EDTA, and 0.5% 0.002). Physical examination of the P0 neonates revealed a class of SDS), digestion with proteinase K overnight at 558C, and extraction as neonate that was either dead or dying within the first 12 hr after described in Hogan et al. (1986). Briefly, the DNA was extracted once birth. All of these neonates, except one, lacked milk in their with an equal volume of phenol (equilibrated with Tris, pH 8.0) and once with phenol/chloroform (1:1); sodium acetate, pH 6.0, was added to a stomachs (Fig. 1). This explains the difference in weight between final concentration of 0.3 M. DNA was precipitated with an equal volume the Lc/Lc homozygotes and their littermates, because all of these of 100% ethanol, washed in 70% ethanol, and air-dried. The DNA was animals were found to be Lc/Lc when genotyped. We performed resuspended in TE buffer (10 mM Tris, pH 8.0, and 1 mM EDTA). autopsies on all of the dead neonates and found that the major Histological examination of paraffin-embedded embryos and P0 neonates. Embryos were dissected from decidua at days 12.5, 15.5, and 16.5. organs were present and that they were morphologically normal Neonates were collected at P0. They were fixed in Bouin’s fixative (data not shown). overnight at 48C. They were stored in 70% ethanol and then dehydrated through an ethanol series, cleared in toluene, embedded in paraffin, sectioned at 5 mm, and stained with hematoxylin and eosin. Extensive neuron loss in P0 Lc/Lc midbrain Cell Counts. Cells from P0 1/1, Lc/1, and Lc/Lc mice were counted on and hindbrain 50 mm sections of brainstem stained with hematoxylin and eosin. Cell counts The failure of Lc/Lc neonates to feed and the cerebellar pheno- were made at 4003 magnification on sagittal sections at two locations: in the inferior colliculus and in the pons between the trigeminal motor nucleus and type of Lc/1 animals suggested that a possible neuronal deficit in the cerebellum. An objective micrometer and eyepiece reticle were used to homozygous animals may be responsible for their phenotype. To 2 calibrate a 6400 mm field for cell counts. Two fields in each of the designated address this possibility, we undertook an in-depth analysis of the areas on two serial sections from each animal were counted. Cell counts were made from four 1/1, four Lc/1, and four Lc/Lc neonates.
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