Microlissencephaly

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Microlissencephaly
MLIS TUBB2B (cropped).jpg
Microlissencephaly in a 27 WG (week of gestation) foetus with TUBB2B mutation. Macroscopical view of the left hemisphere showing agyria, absent sylvian fissure and absent olfactory bulb.
Specialty Neurology
Types Norman-Roberts syndrome, Barth syndrome, MLIS3, MLIS4
CausesGenetic or viral

Microlissencephaly (MLIS) is a rare congenital brain disorder that combines severe microcephaly (small head) with lissencephaly (smooth brain surface due to absent sulci and gyri). Microlissencephaly is a heterogeneous disorder, i.e. it has many different causes and a variable clinical course. [1] Microlissencephaly is a malformation of cortical development (MCD) that occurs due to failure of neuronal migration between the third and fifth month of gestation as well as stem cell population abnormalities. [2] [3] Numerous genes have been found to be associated with microlissencephaly, however, the pathophysiology is still not completely understood.

Contents

The combination of lissencephaly with severe congenital microcephaly is designated as microlissencephaly only when the cortex is abnormally thick. If such combination exists with a normal cortical thickness (2.5 to 3 mm [4] ), it is known as "microcephaly with simplified gyral pattern" (MSGP). [5] Both MLIS and MSGP have a much more severe clinical course than microcephaly alone. [6] They are inherited in autosomal recessive manner. [7] Prior to 2000, the term "microlissencephaly" was used to designate both MLIS and MSGP. [8]

Types

Microlissencephaly is one of five subtypes of lissencephaly. [9] Microlissencephaly, in turn, can be subclassified based on imaging and clinical picture into four types: [7] [10] [11]

MLIS1

Microlissencephaly Type A or Norman–Roberts syndrome (NRS): a microlissencephaly with thick cortex without infratentorial anomalies.[ citation needed ]

Other clinical features may include: a bitemporal narrowing, a broad nasal root. There is postnatal growth retardation, severe mental retardation associated with pyramidal spasticity and epilepsy. This entity could be identical to "lissencephaly with cerebellar hypoplasia type B" (LCHb), and therefore linked to mutations in RELN gene. [12]

MLIS2

Microlissencephaly Type B or Barth microlissencephaly syndrome: is a microlissencephaly with thick cortex, severe cerebellar and brainstem hypoplasia. The Barth-type of MLIS is the most severe of all the known lissencephaly syndromes.[ citation needed ]

This phenotype consists of polyhydramnios (probably due to poor fetal swallowing), severe congenital microcephaly, weak respiratory effort, and survival for only a few hours or days. [13] Barth described two siblings with this type as having a very low brainweight, wide ventricles, a very thin neopallium, absent corpus callosum and absent olfactory nerve. [14]

MLIS3

Microlissencephaly with intermediate cortex and abrupt anteroposterior gradient[ citation needed ]

MLIS4

Microlissencephaly with mildly to moderately thick (6–8 mm) cortex, callosal agenesis [ citation needed ]

Presentation

MRI of a patient with a TUBA1A mutation showing microlissencephaly with cerebellar hypoplasia. a. smooth brain surface (arrow) b. absent corpus callosum (arrow). Microlissencephaly (cropped).gif
MRI of a patient with a TUBA1A mutation showing microlissencephaly with cerebellar hypoplasia. a. smooth brain surface (arrow) b. absent corpus callosum (arrow).

Microlissencephalic patients suffer from spasticity, seizures, severe developmental delay and intellectual disabilities with survival varying from days to years. Patients may also have dysmorphic craniofacial features, abnormal genitalia, and arthrogryposis. [8] [15] [16]

Microlissencephaly may arise as a part of Baraitser-Winter syndrome which comprises also ptosis, coloboma, hearing loss and learning disability. [17] Moreover, it is the distinct developmental brain abnormality in "microcephalic osteodysplastic primordial dwarfism" (MOPD1). [18] Microlissencephaly may be accompanied by micromelia as in Basel-Vanagaite-Sirota syndrome (a.k.a. Microlissencephaly-Micromelia syndrome).[ citation needed ]

Pathophysiology

Genes associated with MLIS
GeneLocationOMIM number
RELN 7q22.1 600514
CIT 12q24.23 605629
NDE1 16p13.11 609449
KATNB1 16q21 602703
WDR62 19q13.12 613583
ACTG1 17q25.3 102560
TUBA1A 12q13.12 602529
TUBB2B 6p25.2 612850
TUBB3 16q24.3 602661
TUBA3E 2q21.1N/A
TUBG1 17q21.2 191135
DMRTA2 1p32.3 614804

The genetic basis and pathophysiology of microlissencephaly are still not completely understood. [19] Most cases of microlissencephaly are described in consanguineous families suggesting an autosomal recessive inheritance. [7] [20] [16] Mutation of RELN gene or CIT could cause MLIS. [21] [16] [22] Human NDE1 mutations and mouse Nde1 loss lead to cortical lamination deficits, which, together with reduced neuronal production cause microlissencephaly. Homozygous frameshift mutations in NDE1 gene was found to cause microlissencephaly with up to 90% reduction in brain mass and seizures starting early in life. [23] [24] [25] [26] Some other disease-causing genes include: KATNB1 and WDR62 . It is hypothesized that the KATNB1-associated microlissencephaly is the result of a combined effect of reduced neural progenitor populations and impaired interaction between the Katanin P80 subunit (encoded by KATNB1) and LIS1 (a.k.a. PAFAH1B1 ), a protein mutated in type 1 lissencephaly. [27] Missense mutation in ACTG1 gene was identified in three cases of microlissencephaly. ACTG1 is the same gene that, when mutated, causes Baraitser-Winter syndrome. [28] A loss-of-function mutation in the Doublesex- and Mab-3–Related Transcription factor A2 (DMRTA2, also known as DMRT5) gene has been reported in a case of microlissencephaly, implicating DMRTA2 as a critical regulator of cortical neural progenitor cell dynamics. [29]

Microlissencepahly is considered a tubulinopathy (tubulin gene defect) [30] i.e. is caused by mutation in tubulin genes, mainly TUBA1A [31] and less commonly TUBB2B , TUBB3 , TUBA3E and TUBG1 . [32] Central pachygyria, polymicrogyria are more commonly seen in patients with defects in TUBB2B, TUBB3, and TUBB5 . [33] This implys the critical role of microtubule cytoskeleton in the pathophysiology of microlissencephaly as well as other neuronal migration disorders. [20]

Congenital infections like cytomegalovirus are also known to cause microlissencephaly. [16]

Both microlissencephaly and microcephaly with simplified gyral pattern result from either decreased stem cell proliferation or increased apoptosis in the germinal zone of the cerebral cortex. [2]

Diagnosis

Microlissencephaly can be diagnosed by prenatal MRI. [30] MRI is better than ultrasound when it comes to detecting microlissencephaly or MSGP prenatally. [34] The ideal time for proper prenatal diagnosis is between the 34th and 35th gestational week which is the time when the secondary gyration normally terminates. In microlissencephaly cases, the primary sulci would be unusually wide and flat while secondary sulci would be missing. [35]

At birth, lissencephaly with a head circumference of less than minus three standard deviations (< –3 SD) is considered microlissencephaly. [36]

Although genetic diagnosis in patients with MLIS is challenging, exome sequencing has been suggested to be a powerful diagnostic tool. [28]

Dobyns-Barkovich classification

In 1999, Dobyns and Barkovich suggested a classification of patients with severe microcephaly combined with gyral abnormalities including: microcephaly with simplified gyral pattern (MSGP), microlissencephaly and polymicrogyria. The classification divided those patients into ten groups in which MSGP represented the first four groups, microlissencephaly referred to the groups from 5-8 and polymicrogyria in the last two groups. [37]

In Dobyns-Barkovich classification, Dobyns-Barkovich type 6 is equivalent to Norman-Roberts syndrome (MLIS1) while Dobyns-Barkovich type 8 corresponds to Barth microlissencephaly syndrome (MLIS2). [37] [38]

Differential diagnosis

Microlissencephaly is considered a more severe form than microcephaly with simplified gyral pattern. Microlissencephaly is characterized by a smooth cortical surface (absent sulci and gyri) with a thickened cortex (> 3 mm) and is usually associated with other congenital anomalies. Microcephaly with a simplified gyral pattern has too few sulci and normal cortical thickness (3 mm) and is usually an isolated anomaly. [2]

Microlissencephaly and microcephaly with simplified gyral pattern
MicrolissencephalyMSGP
Mode of inheritance (if genetic)Autosomal recessive
Cortical thicknessthickened (>3 mm)normal (3 mm)
Cortical surfacesmoothtoo few sulci
SeveritySevere formMild form
Associated anomalies?usually presentnot present (MSGP is usually isolated)

Prognosis

Many patients will die within the first 10 years of life. [39]

Epidemiology

Microlissencephaly is listed in Orphanet database as a rare disease. [15] There is not much information available about the epidemiology of microlissencepahly in literature. A PhD thesis has estimated the prevalence of microlissencepahly in southeastern Hungary between July 1992 and June 2006 to be a case every 91,000 live births (0.11:10,000). [40]

History

In 1976, the first syndrome with MLIS was reported, now known as Norman–Roberts syndrome (MLIS type A). [41] The Barth type (MLIS type B) was for the first time described in 1982 in two siblings who died soon after birth. [14]

Related Research Articles

<span class="mw-page-title-main">Cerebral cortex</span> Outer layer of the cerebrum of the mammalian brain

The cerebral cortex, also known as the cerebral mantle, is the outer layer of neural tissue of the cerebrum of the brain in humans and other mammals. The cerebral cortex mostly consists of the six-layered neocortex, with just 10% consisting of the allocortex. It is separated into two cortices, by the longitudinal fissure that divides the cerebrum into the left and right cerebral hemispheres. The two hemispheres are joined beneath the cortex by the corpus callosum. The cerebral cortex is the largest site of neural integration in the central nervous system. It plays a key role in attention, perception, awareness, thought, memory, language, and consciousness. The cerebral cortex is part of the brain responsible for cognition.

<span class="mw-page-title-main">Lissencephaly</span> Medical condition

Lissencephaly is a set of rare brain disorders whereby the whole or parts of the surface of the brain appear smooth. It is caused by defective neuronal migration during the 12th to 24th weeks of gestation resulting in a lack of development of brain folds (gyri) and grooves (sulci). It is a form of cephalic disorder. Terms such as agyria and pachygyria are used to describe the appearance of the surface of the brain.

<span class="mw-page-title-main">Microcephaly</span> Condition in which the head is small due to an underdeveloped brain

Microcephaly is a medical condition involving a smaller-than-normal head. Microcephaly may be present at birth or it may develop in the first few years of life. Brain development is often affected; people with this disorder often have an intellectual disability, poor motor function, poor speech, abnormal facial features, seizures and dwarfism.

Miller–Dieker syndrome, Miller–Dieker lissencephaly syndrome (MDLS), and chromosome 17p13.3 deletion syndrome is a micro deletion syndrome characterized by congenital malformations. Congenital malformations are physical defects detectable in an infant at birth which can involve many different parts of the body including the brain, hearts, lungs, liver, bones, or intestinal tract. MDS is a contiguous gene syndrome – a disorder due to the deletion of multiple gene loci adjacent to one another. The disorder arises from the deletion of part of the small arm of chromosome 17p, leading to partial monosomy. There may be unbalanced translocations, or the presence of a ring chromosome 17.

<span class="mw-page-title-main">Polymicrogyria</span> Medical condition

Polymicrogyria (PMG) is a condition that affects the development of the human brain by multiple small gyri (microgyri) creating excessive folding of the brain leading to an abnormally thick cortex. This abnormality can affect either one region of the brain or multiple regions.

Bilateral frontoparietal polymicrogyria is a genetic disorder with autosomal recessive inheritance that causes a cortical malformation. Our brain has folds in the cortex to increase surface area called gyri and patients with polymicrogyria have an increase number of folds and smaller folds than usual. Polymicrogyria is defined as a cerebral malformation of cortical development in which the normal gyral pattern of the surface of the brain is replaced by an excessive number of small, fused gyri separated by shallow sulci and abnormal cortical lamination. From ongoing research, mutation in GPR56, a member of the adhesion G protein-coupled receptor (GPCR) family, results in BFPP. These mutations are located in different regions of the protein without any evidence of a relationship between the position of the mutation and phenotypic severity. It is also found that GPR56 plays a role in cortical pattering.

<span class="mw-page-title-main">Gyrus</span> Ridge on the cerebral cortex of the brain

In neuroanatomy, a gyrus is a ridge on the cerebral cortex. It is generally surrounded by one or more sulci. Gyri and sulci create the folded appearance of the brain in humans and other mammals.

Pachygyria is a congenital malformation of the cerebral hemisphere. It results in unusually thick convolutions of the cerebral cortex. Typically, children have developmental delay and seizures, the onset and severity depending on the severity of the cortical malformation. Infantile spasms are common in affected children, as is intractable epilepsy.

<span class="mw-page-title-main">Radial glial cell</span> Bipolar-shaped progenitor cells of all neurons in the cerebral cortex and some glia

Radial glial cells, or radial glial progenitor cells (RGPs), are bipolar-shaped progenitor cells that are responsible for producing all of the neurons in the cerebral cortex. RGPs also produce certain lineages of glia, including astrocytes and oligodendrocytes. Their cell bodies (somata) reside in the embryonic ventricular zone, which lies next to the developing ventricular system.

<span class="mw-page-title-main">Doublecortin</span> Protein-coding gene in humans

Neuronal migration protein doublecortin, also known as doublin or lissencephalin-X is a protein that in humans is encoded by the DCX gene.

<span class="mw-page-title-main">PAFAH1B1</span> Protein-coding gene in the species Homo sapiens

Platelet-activating factor acetylhydrolase IB subunit alpha is an enzyme that in humans is encoded by the PAFAH1B1 gene. The protein is often referred to as Lis1 and plays an important role in regulating the motor protein Dynein.

<span class="mw-page-title-main">Tubulin alpha-1A chain</span> Protein-coding gene in the species Homo sapiens

Tubulin alpha-1A chain is a protein that in humans is encoded by the TUBA1A gene.

<span class="mw-page-title-main">WDR62</span> Protein-coding gene in the species Homo sapiens

WD repeat-containing protein 62 is a protein that in humans is encoded by the WDR62 gene.

Gyrification is the process of forming the characteristic folds of the cerebral cortex.

<span class="mw-page-title-main">Neuronal migration disorder</span> Medical condition

Neuronal migration disorder (NMD) refers to a heterogenous group of disorders that, it is supposed, share the same etiopathological mechanism: a variable degree of disruption in the migration of neuroblasts during neurogenesis. The neuronal migration disorders are termed cerebral dysgenesis disorders, brain malformations caused by primary alterations during neurogenesis; on the other hand, brain malformations are highly diverse and refer to any insult to the brain during its formation and maturation due to intrinsic or extrinsic causes that ultimately will alter the normal brain anatomy. However, there is some controversy in the terminology because virtually any malformation will involve neuroblast migration, either primarily or secondarily.

The development of the cerebral cortex, known as corticogenesis is the process during which the cerebral cortex of the brain is formed as part of the development of the nervous system of mammals including its development in humans. The cortex is the outer layer of the brain and is composed of up to six layers. Neurons formed in the ventricular zone migrate to their final locations in one of the six layers of the cortex. The process occurs from embryonic day 10 to 17 in mice and between gestational weeks seven to 18 in humans.

Christopher A. Walsh is the Bullard Professor of Neurology at Harvard Medical School, Chief of the Division of Genetics at Children's Hospital Boston, Investigator of the Howard Hughes Medical Institute, and the former Director of the Harvard–MIT MD–PhD Program. His research focuses on genetics of human cortical development and somatic mutations contributions to human brain diseases.

<span class="mw-page-title-main">Strømme syndrome</span> Rare genetic condition involving intestinal atresia, eye abnormalities and microcephaly

Strømme syndrome is a very rare autosomal recessive genetic condition characterised by intestinal atresia, eye abnormalities and microcephaly. The intestinal atresia is of the "apple-peel" type, in which the remaining intestine is twisted around its main artery. The front third of the eye is typically underdeveloped, and there is usually moderate developmental delay. Less common features include an atrial septal defect, increased muscle tone or skeletal abnormalities. Physical features may include short stature, large, low-set ears, a small jaw, a large mouth, epicanthic folds, or fine, sparse hair.

<span class="mw-page-title-main">Muscle–eye–brain disease</span> Medical condition

Muscle–eye–brain (MEB) disease, also known as muscular dystrophy-dystroglycanopathy congenital with brain and eye anomalies A3 (MDDGA3), is a kind of rare congenital muscular dystrophy (CMD), largely characterized by hypotonia at birth. Patients have muscular dystrophy, central nervous system abnormalities and ocular abnormalities. The condition is degenerative.

David Anthony Keays is an Australian neuroscientist who studies magnetoreception and neurodevelopment. He is currently Chair of Organismal and Developmental Neurobiology at the Ludwig Maximilians University (LMU) in Munich, and a Principle Research Associate at the University of Cambridge. He was formerly a group leader at the Research Institute of Molecular Pathology (IMP) in Vienna, Austria,

References

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